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Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression
Carbon Catabolite repression (CCR) allows a fast adaptation of Bacteria to changing nutrient supplies. The Pseudomonas aeruginosa (PAO1) catabolite repression control protein (Crc) was deemed to act as a translational regulator, repressing functions involved in uptake and utilization of carbon sourc...
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Published in: | PLoS genetics 2014-06, Vol.10 (6), p.e1004440-e1004440 |
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description | Carbon Catabolite repression (CCR) allows a fast adaptation of Bacteria to changing nutrient supplies. The Pseudomonas aeruginosa (PAO1) catabolite repression control protein (Crc) was deemed to act as a translational regulator, repressing functions involved in uptake and utilization of carbon sources. However, Crc of PAO1 was recently shown to be devoid of RNA binding activity. In this study the RNA chaperone Hfq was identified as the principle post-transcriptional regulator of CCR in PAO1. Hfq is shown to bind to A-rich sequences within the ribosome binding site of the model mRNA amiE, and to repress translation in vitro and in vivo. We further report that Crc plays an unknown ancillary role, as full-fledged repression of amiE and other CCR-regulated mRNAs in vivo required its presence. Moreover, we show that the regulatory RNA CrcZ, transcription of which is augmented when CCR is alleviated, binds to Hfq with high affinity. This study on CCR in PAO1 revealed a novel concept for Hfq function, wherein the regulatory RNA CrcZ acts as a decoy to abrogate Hfq-mediated translational repression of catabolic genes and thus highlights the central role of RNA based regulation in CCR of PAO1. |
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The Pseudomonas aeruginosa (PAO1) catabolite repression control protein (Crc) was deemed to act as a translational regulator, repressing functions involved in uptake and utilization of carbon sources. However, Crc of PAO1 was recently shown to be devoid of RNA binding activity. In this study the RNA chaperone Hfq was identified as the principle post-transcriptional regulator of CCR in PAO1. Hfq is shown to bind to A-rich sequences within the ribosome binding site of the model mRNA amiE, and to repress translation in vitro and in vivo. We further report that Crc plays an unknown ancillary role, as full-fledged repression of amiE and other CCR-regulated mRNAs in vivo required its presence. Moreover, we show that the regulatory RNA CrcZ, transcription of which is augmented when CCR is alleviated, binds to Hfq with high affinity. This study on CCR in PAO1 revealed a novel concept for Hfq function, wherein the regulatory RNA CrcZ acts as a decoy to abrogate Hfq-mediated translational repression of catabolic genes and thus highlights the central role of RNA based regulation in CCR of PAO1.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1004440</identifier><identifier>PMID: 24945892</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amidohydrolases - antagonists & inhibitors ; Amidohydrolases - genetics ; Amidohydrolases - metabolism ; Analysis ; Bacteria ; Bacteriology ; Binding sites ; Biology and Life Sciences ; Carbon ; Carbon - metabolism ; Catabolite Repression - genetics ; Experiments ; Gene Expression Regulation, Bacterial ; Genetic aspects ; Genetic regulation ; Host Factor 1 Protein - genetics ; Physiological aspects ; Proteins ; Pseudomonas aeruginosa ; Pseudomonas aeruginosa - genetics ; Pseudomonas aeruginosa - metabolism ; Pseudomonas Infections ; Regulation ; Regulatory Sequences, Ribonucleic Acid - genetics ; Ribosomes - metabolism ; RNA ; RNA Processing, Post-Transcriptional ; RNA, Bacterial - genetics ; RNA, Messenger - genetics ; RNA-Binding Proteins - genetics ; Scholarships & fellowships ; Signal transduction ; Standard deviation</subject><ispartof>PLoS genetics, 2014-06, Vol.10 (6), p.e1004440-e1004440</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Sonnleitner, Bläsi 2014 Sonnleitner, Bläsi</rights><rights>2014 Sonnleitner, Bläsi. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Sonnleitner E, Bläsi U (2014) Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa Carbon Catabolite Repression. PLoS Genet 10(6): e1004440. doi:10.1371/journal.pgen.1004440</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c764t-3820bc70caa44b543d369c4a51003b8fa03fef07eeea978bfe28f79b5d75bb9b3</citedby><cites>FETCH-LOGICAL-c764t-3820bc70caa44b543d369c4a51003b8fa03fef07eeea978bfe28f79b5d75bb9b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4063720/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4063720/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,37013,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24945892$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Garsin, Danielle A.</contributor><creatorcontrib>Sonnleitner, Elisabeth</creatorcontrib><creatorcontrib>Bläsi, Udo</creatorcontrib><title>Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Carbon Catabolite repression (CCR) allows a fast adaptation of Bacteria to changing nutrient supplies. The Pseudomonas aeruginosa (PAO1) catabolite repression control protein (Crc) was deemed to act as a translational regulator, repressing functions involved in uptake and utilization of carbon sources. However, Crc of PAO1 was recently shown to be devoid of RNA binding activity. In this study the RNA chaperone Hfq was identified as the principle post-transcriptional regulator of CCR in PAO1. Hfq is shown to bind to A-rich sequences within the ribosome binding site of the model mRNA amiE, and to repress translation in vitro and in vivo. We further report that Crc plays an unknown ancillary role, as full-fledged repression of amiE and other CCR-regulated mRNAs in vivo required its presence. Moreover, we show that the regulatory RNA CrcZ, transcription of which is augmented when CCR is alleviated, binds to Hfq with high affinity. This study on CCR in PAO1 revealed a novel concept for Hfq function, wherein the regulatory RNA CrcZ acts as a decoy to abrogate Hfq-mediated translational repression of catabolic genes and thus highlights the central role of RNA based regulation in CCR of PAO1.</description><subject>Amidohydrolases - antagonists & inhibitors</subject><subject>Amidohydrolases - genetics</subject><subject>Amidohydrolases - metabolism</subject><subject>Analysis</subject><subject>Bacteria</subject><subject>Bacteriology</subject><subject>Binding sites</subject><subject>Biology and Life Sciences</subject><subject>Carbon</subject><subject>Carbon - metabolism</subject><subject>Catabolite Repression - genetics</subject><subject>Experiments</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genetic aspects</subject><subject>Genetic regulation</subject><subject>Host Factor 1 Protein - genetics</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>Pseudomonas aeruginosa</subject><subject>Pseudomonas aeruginosa - genetics</subject><subject>Pseudomonas aeruginosa - metabolism</subject><subject>Pseudomonas Infections</subject><subject>Regulation</subject><subject>Regulatory Sequences, Ribonucleic Acid - genetics</subject><subject>Ribosomes - metabolism</subject><subject>RNA</subject><subject>RNA Processing, Post-Transcriptional</subject><subject>RNA, Bacterial - genetics</subject><subject>RNA, Messenger - genetics</subject><subject>RNA-Binding Proteins - genetics</subject><subject>Scholarships & fellowships</subject><subject>Signal transduction</subject><subject>Standard deviation</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNqVk12L1DAUhoso7rr6D0QLgujFjGmTTpqbhWFQd2DZlfED8SacpCedDJ1mNmnF_femzuwyBS-UXCScPO-b5JycJHmekWlGefZu43rfQjPd1dhOM0IYY-RBcpoVBZ1wRtjDo_VJ8iSEDSG0KAV_nJzkTLC4zE-T7yus-wY669rUmfTC3KTqNu3WmK6u5unC6x-pbdNPAfvKbV0LIQX0fW1bFyDV4FXUaehAucZ2mHrceQwhuj1NHhloAj47zGfJ1w_vvywuJpfXH5eL-eVE8xnrJrTMidKcaADGVMFoRWdCMyjii6gqDRBq0BCOiCB4qQzmpeFCFRUvlBKKniUv9767xgV5SEqQWcF4IWguRCSWe6JysJE7b7fgb6UDK_8EnK8l-M7qBiXnZQllnpWCaVZSEMRwSnIoidZVporodX44rVdbrDS2nYdmZDreae1a1u6nZGRGeU6iwZuDgXc3PYZObm3Q2DTQouuHe1PBYsmyLKKv9mgN8Wq2NS466gGX85g2UUTLgZr-hYqjwq3VrkVjY3wkeDsSRKbDX10NfQhy-Xn1H-zVv7PX38bs6yN2jdB06-CafviGYQyyPai9C8GjuU91RuTQBncVl0MbyEMbRNmL4zLdi-7-Pf0NxKIBig</recordid><startdate>20140601</startdate><enddate>20140601</enddate><creator>Sonnleitner, Elisabeth</creator><creator>Bläsi, Udo</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140601</creationdate><title>Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression</title><author>Sonnleitner, Elisabeth ; Bläsi, Udo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c764t-3820bc70caa44b543d369c4a51003b8fa03fef07eeea978bfe28f79b5d75bb9b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Amidohydrolases - antagonists & inhibitors</topic><topic>Amidohydrolases - genetics</topic><topic>Amidohydrolases - metabolism</topic><topic>Analysis</topic><topic>Bacteria</topic><topic>Bacteriology</topic><topic>Binding sites</topic><topic>Biology and Life Sciences</topic><topic>Carbon</topic><topic>Carbon - metabolism</topic><topic>Catabolite Repression - genetics</topic><topic>Experiments</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genetic aspects</topic><topic>Genetic regulation</topic><topic>Host Factor 1 Protein - genetics</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>Pseudomonas aeruginosa</topic><topic>Pseudomonas aeruginosa - genetics</topic><topic>Pseudomonas aeruginosa - metabolism</topic><topic>Pseudomonas Infections</topic><topic>Regulation</topic><topic>Regulatory Sequences, Ribonucleic Acid - genetics</topic><topic>Ribosomes - metabolism</topic><topic>RNA</topic><topic>RNA Processing, Post-Transcriptional</topic><topic>RNA, Bacterial - genetics</topic><topic>RNA, Messenger - genetics</topic><topic>RNA-Binding Proteins - genetics</topic><topic>Scholarships & fellowships</topic><topic>Signal transduction</topic><topic>Standard deviation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sonnleitner, Elisabeth</creatorcontrib><creatorcontrib>Bläsi, Udo</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints database</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sonnleitner, Elisabeth</au><au>Bläsi, Udo</au><au>Garsin, Danielle A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2014-06-01</date><risdate>2014</risdate><volume>10</volume><issue>6</issue><spage>e1004440</spage><epage>e1004440</epage><pages>e1004440-e1004440</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Carbon Catabolite repression (CCR) allows a fast adaptation of Bacteria to changing nutrient supplies. The Pseudomonas aeruginosa (PAO1) catabolite repression control protein (Crc) was deemed to act as a translational regulator, repressing functions involved in uptake and utilization of carbon sources. However, Crc of PAO1 was recently shown to be devoid of RNA binding activity. In this study the RNA chaperone Hfq was identified as the principle post-transcriptional regulator of CCR in PAO1. Hfq is shown to bind to A-rich sequences within the ribosome binding site of the model mRNA amiE, and to repress translation in vitro and in vivo. We further report that Crc plays an unknown ancillary role, as full-fledged repression of amiE and other CCR-regulated mRNAs in vivo required its presence. Moreover, we show that the regulatory RNA CrcZ, transcription of which is augmented when CCR is alleviated, binds to Hfq with high affinity. This study on CCR in PAO1 revealed a novel concept for Hfq function, wherein the regulatory RNA CrcZ acts as a decoy to abrogate Hfq-mediated translational repression of catabolic genes and thus highlights the central role of RNA based regulation in CCR of PAO1.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24945892</pmid><doi>10.1371/journal.pgen.1004440</doi><oa>free_for_read</oa></addata></record> |
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subjects | Amidohydrolases - antagonists & inhibitors Amidohydrolases - genetics Amidohydrolases - metabolism Analysis Bacteria Bacteriology Binding sites Biology and Life Sciences Carbon Carbon - metabolism Catabolite Repression - genetics Experiments Gene Expression Regulation, Bacterial Genetic aspects Genetic regulation Host Factor 1 Protein - genetics Physiological aspects Proteins Pseudomonas aeruginosa Pseudomonas aeruginosa - genetics Pseudomonas aeruginosa - metabolism Pseudomonas Infections Regulation Regulatory Sequences, Ribonucleic Acid - genetics Ribosomes - metabolism RNA RNA Processing, Post-Transcriptional RNA, Bacterial - genetics RNA, Messenger - genetics RNA-Binding Proteins - genetics Scholarships & fellowships Signal transduction Standard deviation |
title | Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression |
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