Prokaryotic-style frameshifting in a plant translation system: conservation of an unusual single-tRNA slippage event
Ribosomal frameshifting signals are found in mobile genetic elements, viruses and cellular genes of prokaryotes and eukaryotes. Typically they comprise a slippery sequence, X XXY YYZ, where the frameshift occurs, and a stimulatory mRNA element. Here we studied the influence of host translational env...
Gespeichert in:
Veröffentlicht in: | The EMBO journal 2003-08, Vol.22 (15), p.3941-3950 |
---|---|
Hauptverfasser: | , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 3950 |
---|---|
container_issue | 15 |
container_start_page | 3941 |
container_title | The EMBO journal |
container_volume | 22 |
creator | Napthine, Sawsan Vidakovic, Marijana Girnary, Roseanne Namy, Olivier Brierley, Ian |
description | Ribosomal frameshifting signals are found in mobile genetic elements, viruses and cellular genes of prokaryotes and eukaryotes. Typically they comprise a slippery sequence, X XXY YYZ, where the frameshift occurs, and a stimulatory mRNA element. Here we studied the influence of host translational environment and the identity of slippery sequence‐decoding tRNAs on the frameshift mechanism. By expressing candidate signals in
Escherichia coli
, and in wheatgerm extracts depleted of endogenous tRNAs and supplemented with prokaryotic or eukaryotic tRNA populations, we show that when decoding AAG in the ribosomal A‐site,
E.coli
tRNA
Lys
promotes a highly unusual single‐tRNA slippage event in both prokaryotic and eukaryotic ribosomes. This event does not appear to require slippage of the adjacent P‐site tRNA, although its identity is influential. Conversely, asparaginyl‐tRNA promoted a dual slippage event in either system. Thus, the tRNAs themselves are the main determinants in the selection of single‐ or dual‐tRNA slippage mechanisms. We also show for the first time that prokaryotic tRNA
Asn
is not inherently ‘unslippery’ and induces efficient frameshifting when in the context of a eukaryotic translation system. |
doi_str_mv | 10.1093/emboj/cdg365 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_169038</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>18819407</sourcerecordid><originalsourceid>FETCH-LOGICAL-c6255-98a64d9aa6189d814f2c44d07c08c36f45c164733051990c2fb9ebf8f12e6cff3</originalsourceid><addsrcrecordid>eNqFks1v1DAQxS0EotvCjTOyOHBqqD9iJ0HiUKpSQGWpUKGIi-V17K23iR1sZ2H_e1yyKgUhOFmyf2_mzTwD8AijZxg19ED3C786UO2ScnYHzHDJUUFQxe6CGSIcFyWumx2wG-MKIcTqCt8HO5jUNS5JPQPpLPgrGTY-WVXEtOk0NEH2Ol5ak6xbQuughEMnXYIpSBc7max3MG5i0v1zqLyLOqynS2-gdHB0YxxlB2OWd7pIH-aHMHZ2GORSQ73WLj0A94zson64PffAx1fH50evi9P3J2-ODk8LxQljRVNLXraNlDyP0GbDhqiybFGlUK0oNyVTmJcVpYjhpkGKmEWjF6Y2mGiujKF74MVUdxgXvW5Vbh1kJ4Zg-zyy8NKK31-cvRRLvxaYN4jWWf90qw_-66hjEr2NSnd5G9qPUVSUEUo4-i-I87qbElUZfPIHuPJjcHkJAjcsx1VTnqH9CVLBxxi0uXGMkbjOXPzMXEyZZ_zx7Sl_wduQM8Am4Jvt9OafxcTxu5dvK5atVNeFi0kXs8Qtdbhl9u9GtrzNf-P7TR8ZrgSvaMXExfxEfMGf0Pzs87m4oD8AbN7cQw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>195261836</pqid></control><display><type>article</type><title>Prokaryotic-style frameshifting in a plant translation system: conservation of an unusual single-tRNA slippage event</title><source>MEDLINE</source><source>Wiley Online Library Journals Frontfile Complete</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Wiley Free Content</source><source>PubMed Central</source><source>Free Full-Text Journals in Chemistry</source><creator>Napthine, Sawsan ; Vidakovic, Marijana ; Girnary, Roseanne ; Namy, Olivier ; Brierley, Ian</creator><creatorcontrib>Napthine, Sawsan ; Vidakovic, Marijana ; Girnary, Roseanne ; Namy, Olivier ; Brierley, Ian</creatorcontrib><description>Ribosomal frameshifting signals are found in mobile genetic elements, viruses and cellular genes of prokaryotes and eukaryotes. Typically they comprise a slippery sequence, X XXY YYZ, where the frameshift occurs, and a stimulatory mRNA element. Here we studied the influence of host translational environment and the identity of slippery sequence‐decoding tRNAs on the frameshift mechanism. By expressing candidate signals in
Escherichia coli
, and in wheatgerm extracts depleted of endogenous tRNAs and supplemented with prokaryotic or eukaryotic tRNA populations, we show that when decoding AAG in the ribosomal A‐site,
E.coli
tRNA
Lys
promotes a highly unusual single‐tRNA slippage event in both prokaryotic and eukaryotic ribosomes. This event does not appear to require slippage of the adjacent P‐site tRNA, although its identity is influential. Conversely, asparaginyl‐tRNA promoted a dual slippage event in either system. Thus, the tRNAs themselves are the main determinants in the selection of single‐ or dual‐tRNA slippage mechanisms. We also show for the first time that prokaryotic tRNA
Asn
is not inherently ‘unslippery’ and induces efficient frameshifting when in the context of a eukaryotic translation system.</description><identifier>ISSN: 0261-4189</identifier><identifier>ISSN: 1460-2075</identifier><identifier>EISSN: 1460-2075</identifier><identifier>DOI: 10.1093/emboj/cdg365</identifier><identifier>PMID: 12881428</identifier><identifier>CODEN: EMJODG</identifier><language>eng</language><publisher>Chichester, UK: John Wiley & Sons, Ltd</publisher><subject>Base Sequence ; E coli ; EMBO31 ; Escherichia coli - genetics ; frameshifting ; Frameshifting, Ribosomal ; Molecular Sequence Data ; Nucleic Acid Conformation ; Plants - genetics ; Protein Biosynthesis ; pseudoknot ; ribosome ; RNA, Transfer - chemistry ; RNA, Transfer - genetics ; translation ; tRNA</subject><ispartof>The EMBO journal, 2003-08, Vol.22 (15), p.3941-3950</ispartof><rights>European Molecular Biology Organization 2003</rights><rights>Copyright © 2003 European Molecular Biology Organization</rights><rights>Copyright Oxford University Press(England) Aug 01, 2003</rights><rights>Copyright © 2003 European Molecular Biology Organization 2003</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6255-98a64d9aa6189d814f2c44d07c08c36f45c164733051990c2fb9ebf8f12e6cff3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC169038/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC169038/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,882,1412,1428,27905,27906,45555,45556,46390,46814,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12881428$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Napthine, Sawsan</creatorcontrib><creatorcontrib>Vidakovic, Marijana</creatorcontrib><creatorcontrib>Girnary, Roseanne</creatorcontrib><creatorcontrib>Namy, Olivier</creatorcontrib><creatorcontrib>Brierley, Ian</creatorcontrib><title>Prokaryotic-style frameshifting in a plant translation system: conservation of an unusual single-tRNA slippage event</title><title>The EMBO journal</title><addtitle>EMBO J</addtitle><addtitle>EMBO J</addtitle><description>Ribosomal frameshifting signals are found in mobile genetic elements, viruses and cellular genes of prokaryotes and eukaryotes. Typically they comprise a slippery sequence, X XXY YYZ, where the frameshift occurs, and a stimulatory mRNA element. Here we studied the influence of host translational environment and the identity of slippery sequence‐decoding tRNAs on the frameshift mechanism. By expressing candidate signals in
Escherichia coli
, and in wheatgerm extracts depleted of endogenous tRNAs and supplemented with prokaryotic or eukaryotic tRNA populations, we show that when decoding AAG in the ribosomal A‐site,
E.coli
tRNA
Lys
promotes a highly unusual single‐tRNA slippage event in both prokaryotic and eukaryotic ribosomes. This event does not appear to require slippage of the adjacent P‐site tRNA, although its identity is influential. Conversely, asparaginyl‐tRNA promoted a dual slippage event in either system. Thus, the tRNAs themselves are the main determinants in the selection of single‐ or dual‐tRNA slippage mechanisms. We also show for the first time that prokaryotic tRNA
Asn
is not inherently ‘unslippery’ and induces efficient frameshifting when in the context of a eukaryotic translation system.</description><subject>Base Sequence</subject><subject>E coli</subject><subject>EMBO31</subject><subject>Escherichia coli - genetics</subject><subject>frameshifting</subject><subject>Frameshifting, Ribosomal</subject><subject>Molecular Sequence Data</subject><subject>Nucleic Acid Conformation</subject><subject>Plants - genetics</subject><subject>Protein Biosynthesis</subject><subject>pseudoknot</subject><subject>ribosome</subject><subject>RNA, Transfer - chemistry</subject><subject>RNA, Transfer - genetics</subject><subject>translation</subject><subject>tRNA</subject><issn>0261-4189</issn><issn>1460-2075</issn><issn>1460-2075</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqFks1v1DAQxS0EotvCjTOyOHBqqD9iJ0HiUKpSQGWpUKGIi-V17K23iR1sZ2H_e1yyKgUhOFmyf2_mzTwD8AijZxg19ED3C786UO2ScnYHzHDJUUFQxe6CGSIcFyWumx2wG-MKIcTqCt8HO5jUNS5JPQPpLPgrGTY-WVXEtOk0NEH2Ol5ak6xbQuughEMnXYIpSBc7max3MG5i0v1zqLyLOqynS2-gdHB0YxxlB2OWd7pIH-aHMHZ2GORSQ73WLj0A94zson64PffAx1fH50evi9P3J2-ODk8LxQljRVNLXraNlDyP0GbDhqiybFGlUK0oNyVTmJcVpYjhpkGKmEWjF6Y2mGiujKF74MVUdxgXvW5Vbh1kJ4Zg-zyy8NKK31-cvRRLvxaYN4jWWf90qw_-66hjEr2NSnd5G9qPUVSUEUo4-i-I87qbElUZfPIHuPJjcHkJAjcsx1VTnqH9CVLBxxi0uXGMkbjOXPzMXEyZZ_zx7Sl_wduQM8Am4Jvt9OafxcTxu5dvK5atVNeFi0kXs8Qtdbhl9u9GtrzNf-P7TR8ZrgSvaMXExfxEfMGf0Pzs87m4oD8AbN7cQw</recordid><startdate>20030801</startdate><enddate>20030801</enddate><creator>Napthine, Sawsan</creator><creator>Vidakovic, Marijana</creator><creator>Girnary, Roseanne</creator><creator>Namy, Olivier</creator><creator>Brierley, Ian</creator><general>John Wiley & Sons, Ltd</general><general>Nature Publishing Group UK</general><general>Blackwell Publishing Ltd</general><general>Oxford University Press</general><scope>BSCLL</scope><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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20030801</creationdate><title>Prokaryotic-style frameshifting in a plant translation system: conservation of an unusual single-tRNA slippage event</title><author>Napthine, Sawsan ; Vidakovic, Marijana ; Girnary, Roseanne ; Namy, Olivier ; Brierley, Ian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6255-98a64d9aa6189d814f2c44d07c08c36f45c164733051990c2fb9ebf8f12e6cff3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Base Sequence</topic><topic>E coli</topic><topic>EMBO31</topic><topic>Escherichia coli - genetics</topic><topic>frameshifting</topic><topic>Frameshifting, Ribosomal</topic><topic>Molecular Sequence Data</topic><topic>Nucleic Acid Conformation</topic><topic>Plants - genetics</topic><topic>Protein Biosynthesis</topic><topic>pseudoknot</topic><topic>ribosome</topic><topic>RNA, Transfer - chemistry</topic><topic>RNA, Transfer - genetics</topic><topic>translation</topic><topic>tRNA</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Napthine, Sawsan</creatorcontrib><creatorcontrib>Vidakovic, Marijana</creatorcontrib><creatorcontrib>Girnary, Roseanne</creatorcontrib><creatorcontrib>Namy, Olivier</creatorcontrib><creatorcontrib>Brierley, Ian</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Earth, Atmospheric & Aquatic Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The EMBO journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Napthine, Sawsan</au><au>Vidakovic, Marijana</au><au>Girnary, Roseanne</au><au>Namy, Olivier</au><au>Brierley, Ian</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prokaryotic-style frameshifting in a plant translation system: conservation of an unusual single-tRNA slippage event</atitle><jtitle>The EMBO journal</jtitle><stitle>EMBO J</stitle><addtitle>EMBO J</addtitle><date>2003-08-01</date><risdate>2003</risdate><volume>22</volume><issue>15</issue><spage>3941</spage><epage>3950</epage><pages>3941-3950</pages><issn>0261-4189</issn><issn>1460-2075</issn><eissn>1460-2075</eissn><coden>EMJODG</coden><abstract>Ribosomal frameshifting signals are found in mobile genetic elements, viruses and cellular genes of prokaryotes and eukaryotes. Typically they comprise a slippery sequence, X XXY YYZ, where the frameshift occurs, and a stimulatory mRNA element. Here we studied the influence of host translational environment and the identity of slippery sequence‐decoding tRNAs on the frameshift mechanism. By expressing candidate signals in
Escherichia coli
, and in wheatgerm extracts depleted of endogenous tRNAs and supplemented with prokaryotic or eukaryotic tRNA populations, we show that when decoding AAG in the ribosomal A‐site,
E.coli
tRNA
Lys
promotes a highly unusual single‐tRNA slippage event in both prokaryotic and eukaryotic ribosomes. This event does not appear to require slippage of the adjacent P‐site tRNA, although its identity is influential. Conversely, asparaginyl‐tRNA promoted a dual slippage event in either system. Thus, the tRNAs themselves are the main determinants in the selection of single‐ or dual‐tRNA slippage mechanisms. We also show for the first time that prokaryotic tRNA
Asn
is not inherently ‘unslippery’ and induces efficient frameshifting when in the context of a eukaryotic translation system.</abstract><cop>Chichester, UK</cop><pub>John Wiley & Sons, Ltd</pub><pmid>12881428</pmid><doi>10.1093/emboj/cdg365</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0261-4189 |
ispartof | The EMBO journal, 2003-08, Vol.22 (15), p.3941-3950 |
issn | 0261-4189 1460-2075 1460-2075 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_169038 |
source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley Free Content; PubMed Central; Free Full-Text Journals in Chemistry |
subjects | Base Sequence E coli EMBO31 Escherichia coli - genetics frameshifting Frameshifting, Ribosomal Molecular Sequence Data Nucleic Acid Conformation Plants - genetics Protein Biosynthesis pseudoknot ribosome RNA, Transfer - chemistry RNA, Transfer - genetics translation tRNA |
title | Prokaryotic-style frameshifting in a plant translation system: conservation of an unusual single-tRNA slippage event |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-19T10%3A01%3A42IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Prokaryotic-style%20frameshifting%20in%20a%20plant%20translation%20system:%20conservation%20of%20an%20unusual%20single-tRNA%20slippage%20event&rft.jtitle=The%20EMBO%20journal&rft.au=Napthine,%20Sawsan&rft.date=2003-08-01&rft.volume=22&rft.issue=15&rft.spage=3941&rft.epage=3950&rft.pages=3941-3950&rft.issn=0261-4189&rft.eissn=1460-2075&rft.coden=EMJODG&rft_id=info:doi/10.1093/emboj/cdg365&rft_dat=%3Cproquest_pubme%3E18819407%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=195261836&rft_id=info:pmid/12881428&rfr_iscdi=true |