Two novel members of the LhrC family of small RNAs in Listeria monocytogenes with overlapping regulatory functions but distinctive expression profiles
Multicopy small RNAs (sRNAs) have gained recognition as an important feature of bacterial gene regulation. In the human pathogen Listeria monocytogenes, 5 homologous sRNAs, called LhrC1-5, control gene expression by base pairing to target mRNAs though 3 conserved UCCC motifs common to all 5 LhrCs. W...
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| Veröffentlicht in: | RNA biology 2016-09, Vol.13 (9), p.895-915 |
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| creator | Mollerup, Maria Storm Ross, Joseph Andrew Helfer, Anne-Catherine Meistrup, Kristine Romby, Pascale Kallipolitis, Birgitte Haahr |
| description | Multicopy small RNAs (sRNAs) have gained recognition as an important feature of bacterial gene regulation. In the human pathogen Listeria monocytogenes, 5 homologous sRNAs, called LhrC1-5, control gene expression by base pairing to target mRNAs though 3 conserved UCCC motifs common to all 5 LhrCs. We show here that the sRNAs Rli22 and Rli33-1 are structurally and functionally related to LhrC1-5, expanding the LhrC family to 7 members, which makes it the largest multicopy sRNA family reported so far. Rli22 and Rli33-1 both contain 2 UCCC motifs important for post-transcriptional repression of 3 LhrC target genes. One such target, oppA, encodes a virulence-associated oligo-peptide binding protein. Like LhrC1-5, Rli22 and Rli33-1 employ their UCCC motifs to recognize the Shine-Dalgarno region of oppA mRNA and prevent formation of the ribosomal complex, demonstrating that the 7 sRNAs act in a functionally redundant manner. However, differential expression profiles of the sRNAs under infection-relevant conditions suggest that they might also possess non-overlapping functions. Collectively, this makes the LhrC family a unique case for studying the purpose of sRNA multiplicity in the context of bacterial virulence. |
| doi_str_mv | 10.1080/15476286.2016.1208332 |
| format | Article |
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In the human pathogen Listeria monocytogenes, 5 homologous sRNAs, called LhrC1-5, control gene expression by base pairing to target mRNAs though 3 conserved UCCC motifs common to all 5 LhrCs. We show here that the sRNAs Rli22 and Rli33-1 are structurally and functionally related to LhrC1-5, expanding the LhrC family to 7 members, which makes it the largest multicopy sRNA family reported so far. Rli22 and Rli33-1 both contain 2 UCCC motifs important for post-transcriptional repression of 3 LhrC target genes. One such target, oppA, encodes a virulence-associated oligo-peptide binding protein. Like LhrC1-5, Rli22 and Rli33-1 employ their UCCC motifs to recognize the Shine-Dalgarno region of oppA mRNA and prevent formation of the ribosomal complex, demonstrating that the 7 sRNAs act in a functionally redundant manner. However, differential expression profiles of the sRNAs under infection-relevant conditions suggest that they might also possess non-overlapping functions. Collectively, this makes the LhrC family a unique case for studying the purpose of sRNA multiplicity in the context of bacterial virulence.</description><identifier>ISSN: 1547-6286</identifier><identifier>ISSN: 1555-8584</identifier><identifier>EISSN: 1555-8584</identifier><identifier>DOI: 10.1080/15476286.2016.1208332</identifier><identifier>PMID: 27400116</identifier><language>eng</language><publisher>United States: Taylor & Francis</publisher><subject>animal pathogens ; Antisense ; Base Pairing ; Base Sequence ; binding proteins ; Biochemistry, Molecular Biology ; gene expression ; gene expression regulation ; Gene Expression Regulation, Bacterial ; Gene Order ; genes ; Life Sciences ; Listeria monocytogenes ; Listeria monocytogenes - genetics ; messenger RNA ; Molecular biology ; Multigene Family ; multiplicity ; Nucleic Acid Conformation ; Nucleotide Motifs ; post-transcriptional regulation ; Protein Binding ; Research Paper ; Ribosomes - metabolism ; RNA Interference ; RNA, Bacterial - chemistry ; RNA, Bacterial - genetics ; RNA, Messenger - genetics ; RNA, Small Untranslated - chemistry ; RNA, Small Untranslated - genetics ; sRNAs ; Transcriptome ; virulence</subject><ispartof>RNA biology, 2016-09, Vol.13 (9), p.895-915</ispartof><rights>2016 Taylor & Francis Group, LLC 2016</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2016 Taylor & Francis Group, LLC 2016 Taylor & Francis Group, LLC</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c605t-42c1dee3479dabf16d8b8a877f313b157368ff753c19ce697187496cf2c86ed23</citedby><cites>FETCH-LOGICAL-c605t-42c1dee3479dabf16d8b8a877f313b157368ff753c19ce697187496cf2c86ed23</cites><orcidid>0000-0003-1233-9776</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5013991/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5013991/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27400116$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02294787$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Mollerup, Maria Storm</creatorcontrib><creatorcontrib>Ross, Joseph Andrew</creatorcontrib><creatorcontrib>Helfer, Anne-Catherine</creatorcontrib><creatorcontrib>Meistrup, Kristine</creatorcontrib><creatorcontrib>Romby, Pascale</creatorcontrib><creatorcontrib>Kallipolitis, Birgitte Haahr</creatorcontrib><title>Two novel members of the LhrC family of small RNAs in Listeria monocytogenes with overlapping regulatory functions but distinctive expression profiles</title><title>RNA biology</title><addtitle>RNA Biol</addtitle><description>Multicopy small RNAs (sRNAs) have gained recognition as an important feature of bacterial gene regulation. In the human pathogen Listeria monocytogenes, 5 homologous sRNAs, called LhrC1-5, control gene expression by base pairing to target mRNAs though 3 conserved UCCC motifs common to all 5 LhrCs. We show here that the sRNAs Rli22 and Rli33-1 are structurally and functionally related to LhrC1-5, expanding the LhrC family to 7 members, which makes it the largest multicopy sRNA family reported so far. Rli22 and Rli33-1 both contain 2 UCCC motifs important for post-transcriptional repression of 3 LhrC target genes. One such target, oppA, encodes a virulence-associated oligo-peptide binding protein. Like LhrC1-5, Rli22 and Rli33-1 employ their UCCC motifs to recognize the Shine-Dalgarno region of oppA mRNA and prevent formation of the ribosomal complex, demonstrating that the 7 sRNAs act in a functionally redundant manner. However, differential expression profiles of the sRNAs under infection-relevant conditions suggest that they might also possess non-overlapping functions. Collectively, this makes the LhrC family a unique case for studying the purpose of sRNA multiplicity in the context of bacterial virulence.</description><subject>animal pathogens</subject><subject>Antisense</subject><subject>Base Pairing</subject><subject>Base Sequence</subject><subject>binding proteins</subject><subject>Biochemistry, Molecular Biology</subject><subject>gene expression</subject><subject>gene expression regulation</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Gene Order</subject><subject>genes</subject><subject>Life Sciences</subject><subject>Listeria monocytogenes</subject><subject>Listeria monocytogenes - genetics</subject><subject>messenger RNA</subject><subject>Molecular biology</subject><subject>Multigene Family</subject><subject>multiplicity</subject><subject>Nucleic Acid Conformation</subject><subject>Nucleotide Motifs</subject><subject>post-transcriptional regulation</subject><subject>Protein Binding</subject><subject>Research Paper</subject><subject>Ribosomes - metabolism</subject><subject>RNA Interference</subject><subject>RNA, Bacterial - chemistry</subject><subject>RNA, Bacterial - genetics</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Small Untranslated - chemistry</subject><subject>RNA, Small Untranslated - genetics</subject><subject>sRNAs</subject><subject>Transcriptome</subject><subject>virulence</subject><issn>1547-6286</issn><issn>1555-8584</issn><issn>1555-8584</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks-O0zAQxiMEYpeFRwD5CIcW24n_5IKoKpZFqkBCy9lynHFr5NjBTlr6IjzvJmp3BRzgZGvm930zI31F8ZLgJcESvyWsEpxKvqSY8CWhWJYlfVRcEsbYQjJZPZ7_lVjM0EXxLOfvGJdc1uxpcUFFhTEh_LL4dXuIKMQ9eNRB10DKKFo07ABtdmmNrO6cP86l3Gnv0dfPq4xcQBuXB0hOoy6GaI5D3EKAjA5u2KHJLHnd9y5sUYLt6PUQ0xHZMZjBxZBRMw6onQzcXNgDgp99gpynHupTtM5Dfl48sdpneHF-r4pv1x9u1zeLzZePn9arzcJwzIZFRQ1pAcpK1K1uLOGtbKSWQtiSlA1hYjrYWsFKQ2oDvBZEiqrmxlIjObS0vCrenXz7semgNRCGpL3qk-t0OqqonfqzE9xObeNeMUzKuiaTwZuTwe4v2c1qo-YaprSuhBT7mX19HpbijxHyoDqXDXivA8QxK1oJwUuJqfgvSiSpOBOcswllJ9SkmHMC-7AGwWqOirqPipqjos5RmXSvfj_9QXWfjQl4fwJcsDF1-hCTb9Wgjz4mm3QwLqvy3zPuAJRy0SQ</recordid><startdate>20160901</startdate><enddate>20160901</enddate><creator>Mollerup, Maria Storm</creator><creator>Ross, Joseph Andrew</creator><creator>Helfer, Anne-Catherine</creator><creator>Meistrup, Kristine</creator><creator>Romby, Pascale</creator><creator>Kallipolitis, Birgitte Haahr</creator><general>Taylor & Francis</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>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-1233-9776</orcidid></search><sort><creationdate>20160901</creationdate><title>Two novel members of the LhrC family of small RNAs in Listeria monocytogenes with overlapping regulatory functions but distinctive expression profiles</title><author>Mollerup, Maria Storm ; Ross, Joseph Andrew ; Helfer, Anne-Catherine ; Meistrup, Kristine ; Romby, Pascale ; Kallipolitis, Birgitte Haahr</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c605t-42c1dee3479dabf16d8b8a877f313b157368ff753c19ce697187496cf2c86ed23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>animal pathogens</topic><topic>Antisense</topic><topic>Base Pairing</topic><topic>Base Sequence</topic><topic>binding proteins</topic><topic>Biochemistry, Molecular Biology</topic><topic>gene expression</topic><topic>gene expression regulation</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Gene Order</topic><topic>genes</topic><topic>Life Sciences</topic><topic>Listeria monocytogenes</topic><topic>Listeria monocytogenes - genetics</topic><topic>messenger RNA</topic><topic>Molecular biology</topic><topic>Multigene Family</topic><topic>multiplicity</topic><topic>Nucleic Acid Conformation</topic><topic>Nucleotide Motifs</topic><topic>post-transcriptional regulation</topic><topic>Protein Binding</topic><topic>Research Paper</topic><topic>Ribosomes - metabolism</topic><topic>RNA Interference</topic><topic>RNA, Bacterial - chemistry</topic><topic>RNA, Bacterial - genetics</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Small Untranslated - chemistry</topic><topic>RNA, Small Untranslated - genetics</topic><topic>sRNAs</topic><topic>Transcriptome</topic><topic>virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mollerup, Maria Storm</creatorcontrib><creatorcontrib>Ross, Joseph Andrew</creatorcontrib><creatorcontrib>Helfer, Anne-Catherine</creatorcontrib><creatorcontrib>Meistrup, Kristine</creatorcontrib><creatorcontrib>Romby, Pascale</creatorcontrib><creatorcontrib>Kallipolitis, Birgitte Haahr</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>RNA biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mollerup, Maria Storm</au><au>Ross, Joseph Andrew</au><au>Helfer, Anne-Catherine</au><au>Meistrup, Kristine</au><au>Romby, Pascale</au><au>Kallipolitis, Birgitte Haahr</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Two novel members of the LhrC family of small RNAs in Listeria monocytogenes with overlapping regulatory functions but distinctive expression profiles</atitle><jtitle>RNA biology</jtitle><addtitle>RNA Biol</addtitle><date>2016-09-01</date><risdate>2016</risdate><volume>13</volume><issue>9</issue><spage>895</spage><epage>915</epage><pages>895-915</pages><issn>1547-6286</issn><issn>1555-8584</issn><eissn>1555-8584</eissn><abstract>Multicopy small RNAs (sRNAs) have gained recognition as an important feature of bacterial gene regulation. In the human pathogen Listeria monocytogenes, 5 homologous sRNAs, called LhrC1-5, control gene expression by base pairing to target mRNAs though 3 conserved UCCC motifs common to all 5 LhrCs. We show here that the sRNAs Rli22 and Rli33-1 are structurally and functionally related to LhrC1-5, expanding the LhrC family to 7 members, which makes it the largest multicopy sRNA family reported so far. Rli22 and Rli33-1 both contain 2 UCCC motifs important for post-transcriptional repression of 3 LhrC target genes. One such target, oppA, encodes a virulence-associated oligo-peptide binding protein. Like LhrC1-5, Rli22 and Rli33-1 employ their UCCC motifs to recognize the Shine-Dalgarno region of oppA mRNA and prevent formation of the ribosomal complex, demonstrating that the 7 sRNAs act in a functionally redundant manner. However, differential expression profiles of the sRNAs under infection-relevant conditions suggest that they might also possess non-overlapping functions. Collectively, this makes the LhrC family a unique case for studying the purpose of sRNA multiplicity in the context of bacterial virulence.</abstract><cop>United States</cop><pub>Taylor & Francis</pub><pmid>27400116</pmid><doi>10.1080/15476286.2016.1208332</doi><tpages>21</tpages><orcidid>https://orcid.org/0000-0003-1233-9776</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | animal pathogens Antisense Base Pairing Base Sequence binding proteins Biochemistry, Molecular Biology gene expression gene expression regulation Gene Expression Regulation, Bacterial Gene Order genes Life Sciences Listeria monocytogenes Listeria monocytogenes - genetics messenger RNA Molecular biology Multigene Family multiplicity Nucleic Acid Conformation Nucleotide Motifs post-transcriptional regulation Protein Binding Research Paper Ribosomes - metabolism RNA Interference RNA, Bacterial - chemistry RNA, Bacterial - genetics RNA, Messenger - genetics RNA, Small Untranslated - chemistry RNA, Small Untranslated - genetics sRNAs Transcriptome virulence |
| title | Two novel members of the LhrC family of small RNAs in Listeria monocytogenes with overlapping regulatory functions but distinctive expression profiles |
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