Position-dependent termination and widespread obligatory frameshifting in Euplotes translation
Large-scale sequencing approaches reveal that the genetic code of Euplotes ciliates supports widespread ribosomal frameshifting at stop codons, and that additional mechanisms are required for efficient translation termination. The ribosome can change its reading frame during translation in a process...
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| Veröffentlicht in: | Nature structural & molecular biology 2017-01, Vol.24 (1), p.61-68 |
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| creator | Lobanov, Alexei V Heaphy, Stephen M Turanov, Anton A Gerashchenko, Maxim V Pucciarelli, Sandra Devaraj, Raghul R Xie, Fang Petyuk, Vladislav A Smith, Richard D Klobutcher, Lawrence A Atkins, John F Miceli, Cristina Hatfield, Dolph L Baranov, Pavel V Gladyshev, Vadim N |
| description | Large-scale sequencing approaches reveal that the genetic code of
Euplotes
ciliates supports widespread ribosomal frameshifting at stop codons, and that additional mechanisms are required for efficient translation termination.
The ribosome can change its reading frame during translation in a process known as programmed ribosomal frameshifting. These rare events are supported by complex mRNA signals. However, we found that the ciliates
Euplotes crassus
and
Euplotes focardii
exhibit widespread frameshifting at stop codons. 47 different codons preceding stop signals resulted in either +1 or +2 frameshifts, and +1 frameshifting at AAA was the most frequent. The frameshifts showed unusual plasticity and rapid evolution, and had little influence on translation rates. The proximity of a stop codon to the 3′ mRNA end, rather than its occurrence or sequence context, appeared to designate termination. Thus, a 'stop codon' is not a sufficient signal for translation termination, and the default function of stop codons in
Euplotes
is frameshifting, whereas termination is specific to certain mRNA positions and probably requires additional factors. |
| doi_str_mv | 10.1038/nsmb.3330 |
| format | Article |
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Euplotes
ciliates supports widespread ribosomal frameshifting at stop codons, and that additional mechanisms are required for efficient translation termination.
The ribosome can change its reading frame during translation in a process known as programmed ribosomal frameshifting. These rare events are supported by complex mRNA signals. However, we found that the ciliates
Euplotes crassus
and
Euplotes focardii
exhibit widespread frameshifting at stop codons. 47 different codons preceding stop signals resulted in either +1 or +2 frameshifts, and +1 frameshifting at AAA was the most frequent. The frameshifts showed unusual plasticity and rapid evolution, and had little influence on translation rates. The proximity of a stop codon to the 3′ mRNA end, rather than its occurrence or sequence context, appeared to designate termination. Thus, a 'stop codon' is not a sufficient signal for translation termination, and the default function of stop codons in
Euplotes
is frameshifting, whereas termination is specific to certain mRNA positions and probably requires additional factors.</description><identifier>ISSN: 1545-9993</identifier><identifier>EISSN: 1545-9985</identifier><identifier>DOI: 10.1038/nsmb.3330</identifier><identifier>PMID: 27870834</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>631/1647/2017 ; 631/181 ; 631/208/212 ; 631/208/726 ; 631/337/574 ; Amino Acid Sequence ; Base Sequence ; BASIC BIOLOGICAL SCIENCES ; Biochemistry ; Biological Microscopy ; Codons ; Euplotes ; Euplotes - genetics ; Euplotes - metabolism ; Euplotes crassus ; Euplotes focardii ; Frameshift Mutation ; Genetic aspects ; Genetic research ; Genetics ; Life Sciences ; Membrane Biology ; Messenger RNA ; Molecular biology ; Peptide Chain Termination, Translational ; Properties ; Protein Structure ; Proteome - genetics ; Proteome - metabolism ; Protozoan Proteins - genetics ; Protozoan Proteins - metabolism ; Ribonucleic acid ; RNA ; Transcriptome ; Translation (Genetics)</subject><ispartof>Nature structural & molecular biology, 2017-01, Vol.24 (1), p.61-68</ispartof><rights>Springer Nature America, Inc. 2016</rights><rights>COPYRIGHT 2017 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Jan 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c599t-7d0f396f03557fedf34348d63dcff559b2c980255a0611e5e9a92f4cd69077503</citedby><cites>FETCH-LOGICAL-c599t-7d0f396f03557fedf34348d63dcff559b2c980255a0611e5e9a92f4cd69077503</cites><orcidid>0000-0002-2381-2349 ; 0000-0001-9017-0270 ; 0000000190170270 ; 0000000223812349</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nsmb.3330$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nsmb.3330$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27923,27924,41487,42556,51318</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27870834$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1372981$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Lobanov, Alexei V</creatorcontrib><creatorcontrib>Heaphy, Stephen M</creatorcontrib><creatorcontrib>Turanov, Anton A</creatorcontrib><creatorcontrib>Gerashchenko, Maxim V</creatorcontrib><creatorcontrib>Pucciarelli, Sandra</creatorcontrib><creatorcontrib>Devaraj, Raghul R</creatorcontrib><creatorcontrib>Xie, Fang</creatorcontrib><creatorcontrib>Petyuk, Vladislav A</creatorcontrib><creatorcontrib>Smith, Richard D</creatorcontrib><creatorcontrib>Klobutcher, Lawrence A</creatorcontrib><creatorcontrib>Atkins, John F</creatorcontrib><creatorcontrib>Miceli, Cristina</creatorcontrib><creatorcontrib>Hatfield, Dolph L</creatorcontrib><creatorcontrib>Baranov, Pavel V</creatorcontrib><creatorcontrib>Gladyshev, Vadim N</creatorcontrib><creatorcontrib>Pacific Northwest National Lab. (PNNL), Richland, WA (United States)</creatorcontrib><title>Position-dependent termination and widespread obligatory frameshifting in Euplotes translation</title><title>Nature structural & molecular biology</title><addtitle>Nat Struct Mol Biol</addtitle><addtitle>Nat Struct Mol Biol</addtitle><description>Large-scale sequencing approaches reveal that the genetic code of
Euplotes
ciliates supports widespread ribosomal frameshifting at stop codons, and that additional mechanisms are required for efficient translation termination.
The ribosome can change its reading frame during translation in a process known as programmed ribosomal frameshifting. These rare events are supported by complex mRNA signals. However, we found that the ciliates
Euplotes crassus
and
Euplotes focardii
exhibit widespread frameshifting at stop codons. 47 different codons preceding stop signals resulted in either +1 or +2 frameshifts, and +1 frameshifting at AAA was the most frequent. The frameshifts showed unusual plasticity and rapid evolution, and had little influence on translation rates. The proximity of a stop codon to the 3′ mRNA end, rather than its occurrence or sequence context, appeared to designate termination. Thus, a 'stop codon' is not a sufficient signal for translation termination, and the default function of stop codons in
Euplotes
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Heaphy, Stephen M ; Turanov, Anton A ; Gerashchenko, Maxim V ; Pucciarelli, Sandra ; Devaraj, Raghul R ; Xie, Fang ; Petyuk, Vladislav A ; Smith, Richard D ; Klobutcher, Lawrence A ; Atkins, John F ; Miceli, Cristina ; Hatfield, Dolph L ; Baranov, Pavel V ; Gladyshev, Vadim N</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c599t-7d0f396f03557fedf34348d63dcff559b2c980255a0611e5e9a92f4cd69077503</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>631/1647/2017</topic><topic>631/181</topic><topic>631/208/212</topic><topic>631/208/726</topic><topic>631/337/574</topic><topic>Amino Acid Sequence</topic><topic>Base Sequence</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Biochemistry</topic><topic>Biological Microscopy</topic><topic>Codons</topic><topic>Euplotes</topic><topic>Euplotes - genetics</topic><topic>Euplotes - metabolism</topic><topic>Euplotes crassus</topic><topic>Euplotes focardii</topic><topic>Frameshift Mutation</topic><topic>Genetic aspects</topic><topic>Genetic research</topic><topic>Genetics</topic><topic>Life Sciences</topic><topic>Membrane Biology</topic><topic>Messenger RNA</topic><topic>Molecular biology</topic><topic>Peptide Chain Termination, Translational</topic><topic>Properties</topic><topic>Protein Structure</topic><topic>Proteome - genetics</topic><topic>Proteome - metabolism</topic><topic>Protozoan Proteins - genetics</topic><topic>Protozoan Proteins - metabolism</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Transcriptome</topic><topic>Translation (Genetics)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lobanov, Alexei V</creatorcontrib><creatorcontrib>Heaphy, Stephen M</creatorcontrib><creatorcontrib>Turanov, Anton A</creatorcontrib><creatorcontrib>Gerashchenko, Maxim V</creatorcontrib><creatorcontrib>Pucciarelli, Sandra</creatorcontrib><creatorcontrib>Devaraj, Raghul R</creatorcontrib><creatorcontrib>Xie, Fang</creatorcontrib><creatorcontrib>Petyuk, Vladislav A</creatorcontrib><creatorcontrib>Smith, Richard D</creatorcontrib><creatorcontrib>Klobutcher, Lawrence A</creatorcontrib><creatorcontrib>Atkins, John F</creatorcontrib><creatorcontrib>Miceli, Cristina</creatorcontrib><creatorcontrib>Hatfield, Dolph L</creatorcontrib><creatorcontrib>Baranov, Pavel V</creatorcontrib><creatorcontrib>Gladyshev, Vadim N</creatorcontrib><creatorcontrib>Pacific Northwest National Lab. 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(PNNL), Richland, WA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Position-dependent termination and widespread obligatory frameshifting in Euplotes translation</atitle><jtitle>Nature structural & molecular biology</jtitle><stitle>Nat Struct Mol Biol</stitle><addtitle>Nat Struct Mol Biol</addtitle><date>2017-01-01</date><risdate>2017</risdate><volume>24</volume><issue>1</issue><spage>61</spage><epage>68</epage><pages>61-68</pages><issn>1545-9993</issn><eissn>1545-9985</eissn><abstract>Large-scale sequencing approaches reveal that the genetic code of
Euplotes
ciliates supports widespread ribosomal frameshifting at stop codons, and that additional mechanisms are required for efficient translation termination.
The ribosome can change its reading frame during translation in a process known as programmed ribosomal frameshifting. These rare events are supported by complex mRNA signals. However, we found that the ciliates
Euplotes crassus
and
Euplotes focardii
exhibit widespread frameshifting at stop codons. 47 different codons preceding stop signals resulted in either +1 or +2 frameshifts, and +1 frameshifting at AAA was the most frequent. The frameshifts showed unusual plasticity and rapid evolution, and had little influence on translation rates. The proximity of a stop codon to the 3′ mRNA end, rather than its occurrence or sequence context, appeared to designate termination. Thus, a 'stop codon' is not a sufficient signal for translation termination, and the default function of stop codons in
Euplotes
is frameshifting, whereas termination is specific to certain mRNA positions and probably requires additional factors.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>27870834</pmid><doi>10.1038/nsmb.3330</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-2381-2349</orcidid><orcidid>https://orcid.org/0000-0001-9017-0270</orcidid><orcidid>https://orcid.org/0000000190170270</orcidid><orcidid>https://orcid.org/0000000223812349</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 631/1647/2017 631/181 631/208/212 631/208/726 631/337/574 Amino Acid Sequence Base Sequence BASIC BIOLOGICAL SCIENCES Biochemistry Biological Microscopy Codons Euplotes Euplotes - genetics Euplotes - metabolism Euplotes crassus Euplotes focardii Frameshift Mutation Genetic aspects Genetic research Genetics Life Sciences Membrane Biology Messenger RNA Molecular biology Peptide Chain Termination, Translational Properties Protein Structure Proteome - genetics Proteome - metabolism Protozoan Proteins - genetics Protozoan Proteins - metabolism Ribonucleic acid RNA Transcriptome Translation (Genetics) |
| title | Position-dependent termination and widespread obligatory frameshifting in Euplotes translation |
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