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A DEAD-box protein acts through RNA to promote HIV-1 Rev-RRE assembly
The HIV-1 Rev protein activates nuclear export of unspliced and partially spliced viral RNA transcripts, which encode the viral genome and the genes encoding viral structural proteins, by binding to and oligomerizing on the Rev Response Element (RRE). The human DEAD-box protein 1 (DDX1) enhances the...
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| Published in: | Nucleic acids research 2017-05, Vol.45 (8), p.4632-4641 |
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| Main Authors: | , , , , , , , |
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| container_issue | 8 |
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| container_title | Nucleic acids research |
| container_volume | 45 |
| creator | Lamichhane, Rajan Hammond, John A Pauszek, 3rd, Raymond F Anderson, Rae M Pedron, Ingemar van der Schans, Edwin Williamson, James R Millar, David P |
| description | The HIV-1 Rev protein activates nuclear export of unspliced and partially spliced viral RNA transcripts, which encode the viral genome and the genes encoding viral structural proteins, by binding to and oligomerizing on the Rev Response Element (RRE). The human DEAD-box protein 1 (DDX1) enhances the RNA export activity of Rev through an unknown mechanism. Using a single-molecule assembly assay and various DDX1 mutants, we show that DDX1 acts through the RRE RNA to specifically accelerate the nucleation step of the Rev-RRE assembly process. Single-molecule Förster resonance energy transfer (smFRET) experiments using donor-labeled Rev and acceptor-labeled DDX1 show that both proteins can associate with a single RRE molecule. However, simultaneous interaction is only observed in a subset of binding events and does not explain the extent to which DDX1 promotes the nucleation step of Rev-RRE assembly. Together, these results are consistent with a model wherein DDX1 acts as an RNA chaperone, remodeling the RRE into a conformation that is pre-organized to bind the first Rev monomer, thereby promoting the overall Rev-RRE assembly process. |
| doi_str_mv | 10.1093/nar/gkx206 |
| format | article |
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The human DEAD-box protein 1 (DDX1) enhances the RNA export activity of Rev through an unknown mechanism. Using a single-molecule assembly assay and various DDX1 mutants, we show that DDX1 acts through the RRE RNA to specifically accelerate the nucleation step of the Rev-RRE assembly process. Single-molecule Förster resonance energy transfer (smFRET) experiments using donor-labeled Rev and acceptor-labeled DDX1 show that both proteins can associate with a single RRE molecule. However, simultaneous interaction is only observed in a subset of binding events and does not explain the extent to which DDX1 promotes the nucleation step of Rev-RRE assembly. Together, these results are consistent with a model wherein DDX1 acts as an RNA chaperone, remodeling the RRE into a conformation that is pre-organized to bind the first Rev monomer, thereby promoting the overall Rev-RRE assembly process.</description><identifier>ISSN: 0305-1048</identifier><identifier>EISSN: 1362-4962</identifier><identifier>DOI: 10.1093/nar/gkx206</identifier><identifier>PMID: 28379444</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Binding Sites ; Biological Transport ; Carbocyanines - chemistry ; DEAD-box RNA Helicases - genetics ; DEAD-box RNA Helicases - metabolism ; Fluorescence Resonance Energy Transfer ; Fluorescent Dyes - chemistry ; Gene Expression ; Genes, env ; HIV-1 - genetics ; HIV-1 - growth & development ; HIV-1 - metabolism ; Host-Pathogen Interactions ; Humans ; Molecular Biology ; Nucleic Acid Conformation ; Protein Binding ; Recombinant Fusion Proteins - genetics ; Recombinant Fusion Proteins - metabolism ; Rhodamines - chemistry ; RNA, Messenger - chemistry ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; RNA, Viral - chemistry ; RNA, Viral - genetics ; RNA, Viral - metabolism ; Single Molecule Imaging ; Staining and Labeling ; Sulfonic Acids - chemistry ; Virus Assembly - genetics</subject><ispartof>Nucleic acids research, 2017-05, Vol.45 (8), p.4632-4641</ispartof><rights>The Author(s) 2017. Published by Oxford University Press on behalf of Nucleic Acids Research.</rights><rights>The Author(s) 2017. Published by Oxford University Press on behalf of Nucleic Acids Research. 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c378t-c97f01959ab15c194eecc37d073d38ee7e42648593e34b2156b94b9da9b72d6c3</citedby><cites>FETCH-LOGICAL-c378t-c97f01959ab15c194eecc37d073d38ee7e42648593e34b2156b94b9da9b72d6c3</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/PMC5416872/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5416872/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,733,786,790,891,27957,27958,53827,53829</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28379444$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lamichhane, Rajan</creatorcontrib><creatorcontrib>Hammond, John A</creatorcontrib><creatorcontrib>Pauszek, 3rd, Raymond F</creatorcontrib><creatorcontrib>Anderson, Rae M</creatorcontrib><creatorcontrib>Pedron, Ingemar</creatorcontrib><creatorcontrib>van der Schans, Edwin</creatorcontrib><creatorcontrib>Williamson, James R</creatorcontrib><creatorcontrib>Millar, David P</creatorcontrib><title>A DEAD-box protein acts through RNA to promote HIV-1 Rev-RRE assembly</title><title>Nucleic acids research</title><addtitle>Nucleic Acids Res</addtitle><description>The HIV-1 Rev protein activates nuclear export of unspliced and partially spliced viral RNA transcripts, which encode the viral genome and the genes encoding viral structural proteins, by binding to and oligomerizing on the Rev Response Element (RRE). The human DEAD-box protein 1 (DDX1) enhances the RNA export activity of Rev through an unknown mechanism. Using a single-molecule assembly assay and various DDX1 mutants, we show that DDX1 acts through the RRE RNA to specifically accelerate the nucleation step of the Rev-RRE assembly process. Single-molecule Förster resonance energy transfer (smFRET) experiments using donor-labeled Rev and acceptor-labeled DDX1 show that both proteins can associate with a single RRE molecule. However, simultaneous interaction is only observed in a subset of binding events and does not explain the extent to which DDX1 promotes the nucleation step of Rev-RRE assembly. Together, these results are consistent with a model wherein DDX1 acts as an RNA chaperone, remodeling the RRE into a conformation that is pre-organized to bind the first Rev monomer, thereby promoting the overall Rev-RRE assembly process.</description><subject>Binding Sites</subject><subject>Biological Transport</subject><subject>Carbocyanines - chemistry</subject><subject>DEAD-box RNA Helicases - genetics</subject><subject>DEAD-box RNA Helicases - metabolism</subject><subject>Fluorescence Resonance Energy Transfer</subject><subject>Fluorescent Dyes - chemistry</subject><subject>Gene Expression</subject><subject>Genes, env</subject><subject>HIV-1 - genetics</subject><subject>HIV-1 - growth & development</subject><subject>HIV-1 - metabolism</subject><subject>Host-Pathogen Interactions</subject><subject>Humans</subject><subject>Molecular Biology</subject><subject>Nucleic Acid Conformation</subject><subject>Protein Binding</subject><subject>Recombinant Fusion Proteins - genetics</subject><subject>Recombinant Fusion Proteins - metabolism</subject><subject>Rhodamines - chemistry</subject><subject>RNA, Messenger - chemistry</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>RNA, Viral - chemistry</subject><subject>RNA, Viral - genetics</subject><subject>RNA, Viral - metabolism</subject><subject>Single Molecule Imaging</subject><subject>Staining and Labeling</subject><subject>Sulfonic Acids - chemistry</subject><subject>Virus Assembly - genetics</subject><issn>0305-1048</issn><issn>1362-4962</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNpVkEFLwzAcR4Mobk4vfgDJUYS6pEmb5CKUrTphKAz1GtI026ptM5N2bN_ejs2hpxze4_cPD4BrjO4xEmRYKzdcfG1CFJ-APiZxGFARh6egjwiKAowo74EL7z8RwhRH9Bz0Qk6YoJT2QZrAcZqMg8xu4MrZxhQ1VLrxsFk62y6WcPaSwMbuWNVROHn-CDCcmXUwm6VQeW-qrNxegrO5Kr25OrwD8P6Yvo0mwfT16XmUTANNGG8CLdgcYREJleFIY0GN0R3JESM54cYwQ8OY8kgQQ2gW4ijOBM1ErkTGwjzWZAAe9rurNqtMrk3dOFXKlSsq5bbSqkL-J3WxlAu7lhHFMWdhN3B7GHD2uzW-kVXhtSlLVRvbeok5p5RRjkWn3u1V7az3zsyPZzCSu-6y6y733Tv55u_HjupvaPIDPSN97A</recordid><startdate>20170505</startdate><enddate>20170505</enddate><creator>Lamichhane, Rajan</creator><creator>Hammond, John A</creator><creator>Pauszek, 3rd, Raymond F</creator><creator>Anderson, Rae M</creator><creator>Pedron, Ingemar</creator><creator>van der Schans, Edwin</creator><creator>Williamson, James R</creator><creator>Millar, David P</creator><general>Oxford University Press</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>5PM</scope></search><sort><creationdate>20170505</creationdate><title>A DEAD-box protein acts through RNA to promote HIV-1 Rev-RRE assembly</title><author>Lamichhane, Rajan ; Hammond, John A ; Pauszek, 3rd, Raymond F ; Anderson, Rae M ; Pedron, Ingemar ; van der Schans, Edwin ; Williamson, James R ; Millar, David P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c378t-c97f01959ab15c194eecc37d073d38ee7e42648593e34b2156b94b9da9b72d6c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Binding Sites</topic><topic>Biological Transport</topic><topic>Carbocyanines - chemistry</topic><topic>DEAD-box RNA Helicases - genetics</topic><topic>DEAD-box RNA Helicases - metabolism</topic><topic>Fluorescence Resonance Energy Transfer</topic><topic>Fluorescent Dyes - chemistry</topic><topic>Gene Expression</topic><topic>Genes, env</topic><topic>HIV-1 - genetics</topic><topic>HIV-1 - growth & development</topic><topic>HIV-1 - metabolism</topic><topic>Host-Pathogen Interactions</topic><topic>Humans</topic><topic>Molecular Biology</topic><topic>Nucleic Acid Conformation</topic><topic>Protein Binding</topic><topic>Recombinant Fusion Proteins - genetics</topic><topic>Recombinant Fusion Proteins - metabolism</topic><topic>Rhodamines - chemistry</topic><topic>RNA, Messenger - chemistry</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>RNA, Viral - chemistry</topic><topic>RNA, Viral - genetics</topic><topic>RNA, Viral - metabolism</topic><topic>Single Molecule Imaging</topic><topic>Staining and Labeling</topic><topic>Sulfonic Acids - chemistry</topic><topic>Virus Assembly - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lamichhane, Rajan</creatorcontrib><creatorcontrib>Hammond, John A</creatorcontrib><creatorcontrib>Pauszek, 3rd, Raymond F</creatorcontrib><creatorcontrib>Anderson, Rae M</creatorcontrib><creatorcontrib>Pedron, Ingemar</creatorcontrib><creatorcontrib>van der Schans, Edwin</creatorcontrib><creatorcontrib>Williamson, James R</creatorcontrib><creatorcontrib>Millar, David P</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>PubMed Central (Full Participant titles)</collection><jtitle>Nucleic acids research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lamichhane, Rajan</au><au>Hammond, John A</au><au>Pauszek, 3rd, Raymond F</au><au>Anderson, Rae M</au><au>Pedron, Ingemar</au><au>van der Schans, Edwin</au><au>Williamson, James R</au><au>Millar, David P</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A DEAD-box protein acts through RNA to promote HIV-1 Rev-RRE assembly</atitle><jtitle>Nucleic acids research</jtitle><addtitle>Nucleic Acids Res</addtitle><date>2017-05-05</date><risdate>2017</risdate><volume>45</volume><issue>8</issue><spage>4632</spage><epage>4641</epage><pages>4632-4641</pages><issn>0305-1048</issn><eissn>1362-4962</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>The HIV-1 Rev protein activates nuclear export of unspliced and partially spliced viral RNA transcripts, which encode the viral genome and the genes encoding viral structural proteins, by binding to and oligomerizing on the Rev Response Element (RRE). The human DEAD-box protein 1 (DDX1) enhances the RNA export activity of Rev through an unknown mechanism. Using a single-molecule assembly assay and various DDX1 mutants, we show that DDX1 acts through the RRE RNA to specifically accelerate the nucleation step of the Rev-RRE assembly process. Single-molecule Förster resonance energy transfer (smFRET) experiments using donor-labeled Rev and acceptor-labeled DDX1 show that both proteins can associate with a single RRE molecule. However, simultaneous interaction is only observed in a subset of binding events and does not explain the extent to which DDX1 promotes the nucleation step of Rev-RRE assembly. Together, these results are consistent with a model wherein DDX1 acts as an RNA chaperone, remodeling the RRE into a conformation that is pre-organized to bind the first Rev monomer, thereby promoting the overall Rev-RRE assembly process.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>28379444</pmid><doi>10.1093/nar/gkx206</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Nucleic acids research, 2017-05, Vol.45 (8), p.4632-4641 |
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| language | eng |
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| source | Open Access: PubMed Central; Oxford Journals - Connect here FIRST to enable access |
| subjects | Binding Sites Biological Transport Carbocyanines - chemistry DEAD-box RNA Helicases - genetics DEAD-box RNA Helicases - metabolism Fluorescence Resonance Energy Transfer Fluorescent Dyes - chemistry Gene Expression Genes, env HIV-1 - genetics HIV-1 - growth & development HIV-1 - metabolism Host-Pathogen Interactions Humans Molecular Biology Nucleic Acid Conformation Protein Binding Recombinant Fusion Proteins - genetics Recombinant Fusion Proteins - metabolism Rhodamines - chemistry RNA, Messenger - chemistry RNA, Messenger - genetics RNA, Messenger - metabolism RNA, Viral - chemistry RNA, Viral - genetics RNA, Viral - metabolism Single Molecule Imaging Staining and Labeling Sulfonic Acids - chemistry Virus Assembly - genetics |
| title | A DEAD-box protein acts through RNA to promote HIV-1 Rev-RRE assembly |
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