Evidence for Interstrand Quadruplex Formation in the Dimerization of Human Immunodeficiency Virus 1 Genomic RNA
Retroviruses package two homologous single-stranded RNA genomes within a gag protein-RNA complex. In mature virion particles, the two RNA strands are thought to associate primarily through direct RNA-RNA interactions, although the structural basis for this stable association is unknown. We now repor...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 1993-04, Vol.90 (8), p.3393-3397 |
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description | Retroviruses package two homologous single-stranded RNA genomes within a gag protein-RNA complex. In mature virion particles, the two RNA strands are thought to associate primarily through direct RNA-RNA interactions, although the structural basis for this stable association is unknown. We now report that a 127-nucleotide (nt) HIV-1NL4-3RNA fragment (positions 732-858) encompassing the 5' end of the gag gene dimerizes spontaneously under high ionic strength conditions in the absence of any protein cofactor. The HIV-1 RNA dimer is dramatically and specifically stabilized by the monovalent cation potassium. Thermal dissociation of the dimer occurs at 80⚬C in 100 mM K+(5 mM Mg2+) but at significantly lower temperatures in the presence of either smaller or larger monovalent cations (100 mM Li+, 40⚬C; 100 mM Na+, 55⚬C; 100 mM Cs+, 30⚬C). Deletion analyses of the 3' end of the 127-nt fragment reveal that an HIV-1 RNA fragment as short as 94 nt (732-825) can dimerize spontaneously, but a further 9-base deletion of the purine-rich sequence, GGGGGAGAA from positions 817 through 825, eliminates dimerization. These experimental results support a model in which HIV-1 RNA dimerizes by forming an interstrand quadruple helix stabilized by guanine (and/or purine)-base tetrads in analogy to the well-known dimerization of telomeric DNA. We speculate that this structure may also mediate the association of genomic HIV-1 RNA in vivo, revealing how RNA itself can achieve the self-recognition required for subsequent genetic recombination. |
doi_str_mv | 10.1073/pnas.90.8.3393 |
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In mature virion particles, the two RNA strands are thought to associate primarily through direct RNA-RNA interactions, although the structural basis for this stable association is unknown. We now report that a 127-nucleotide (nt) HIV-1NL4-3RNA fragment (positions 732-858) encompassing the 5' end of the gag gene dimerizes spontaneously under high ionic strength conditions in the absence of any protein cofactor. The HIV-1 RNA dimer is dramatically and specifically stabilized by the monovalent cation potassium. Thermal dissociation of the dimer occurs at 80⚬C in 100 mM K+(5 mM Mg2+) but at significantly lower temperatures in the presence of either smaller or larger monovalent cations (100 mM Li+, 40⚬C; 100 mM Na+, 55⚬C; 100 mM Cs+, 30⚬C). Deletion analyses of the 3' end of the 127-nt fragment reveal that an HIV-1 RNA fragment as short as 94 nt (732-825) can dimerize spontaneously, but a further 9-base deletion of the purine-rich sequence, GGGGGAGAA from positions 817 through 825, eliminates dimerization. These experimental results support a model in which HIV-1 RNA dimerizes by forming an interstrand quadruple helix stabilized by guanine (and/or purine)-base tetrads in analogy to the well-known dimerization of telomeric DNA. We speculate that this structure may also mediate the association of genomic HIV-1 RNA in vivo, revealing how RNA itself can achieve the self-recognition required for subsequent genetic recombination.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.90.8.3393</identifier><identifier>PMID: 8475087</identifier><identifier>CODEN: PNASA6</identifier><language>eng</language><publisher>Washington, DC: National Academy of Sciences of the United States of America</publisher><subject>AIDS/HIV ; Base Sequence ; Biochemistry ; Biological and medical sciences ; Cations ; Dimerization ; Dimers ; DNA ; DNA, Viral - genetics ; Drug Stability ; Fundamental and applied biological sciences. Psychology ; Genetics ; Genome, Viral ; Genomics ; HIV ; HIV 1 ; HIV-1 - genetics ; HIV-1 - metabolism ; Human immunodeficiency virus ; human immunodeficiency virus 1 ; Hydrogen Bonding ; Macromolecular Substances ; Microbiology ; Models, Structural ; Molecular Sequence Data ; Monovalent cations ; Nucleic Acid Conformation ; Nucleic acids ; Oligodeoxyribonucleotides ; Polymerase Chain Reaction - methods ; Restriction Mapping ; Ribonucleic acid ; RNA ; RNA, Antisense - genetics ; RNA, Viral - chemistry ; RNA, Viral - genetics ; RNA, Viral - metabolism ; Telomere - physiology ; Thermal stability ; Thermodynamics ; Transcription, Genetic ; Virology</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 1993-04, Vol.90 (8), p.3393-3397</ispartof><rights>Copyright 1993 The National Academy of Sciences of the United States of America</rights><rights>1993 INIST-CNRS</rights><rights>Copyright National Academy of Sciences Apr 15, 1993</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c610t-7e2e71ee6a157dff12a9881bd6be96be78812874219282084ca58ab969bfd0e23</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/90/8.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/2361750$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/2361750$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=4757022$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/8475087$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sundquist, Wesley I.</creatorcontrib><creatorcontrib>Heaphy, Shaun</creatorcontrib><title>Evidence for Interstrand Quadruplex Formation in the Dimerization of Human Immunodeficiency Virus 1 Genomic RNA</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Retroviruses package two homologous single-stranded RNA genomes within a gag protein-RNA complex. In mature virion particles, the two RNA strands are thought to associate primarily through direct RNA-RNA interactions, although the structural basis for this stable association is unknown. We now report that a 127-nucleotide (nt) HIV-1NL4-3RNA fragment (positions 732-858) encompassing the 5' end of the gag gene dimerizes spontaneously under high ionic strength conditions in the absence of any protein cofactor. The HIV-1 RNA dimer is dramatically and specifically stabilized by the monovalent cation potassium. Thermal dissociation of the dimer occurs at 80⚬C in 100 mM K+(5 mM Mg2+) but at significantly lower temperatures in the presence of either smaller or larger monovalent cations (100 mM Li+, 40⚬C; 100 mM Na+, 55⚬C; 100 mM Cs+, 30⚬C). Deletion analyses of the 3' end of the 127-nt fragment reveal that an HIV-1 RNA fragment as short as 94 nt (732-825) can dimerize spontaneously, but a further 9-base deletion of the purine-rich sequence, GGGGGAGAA from positions 817 through 825, eliminates dimerization. These experimental results support a model in which HIV-1 RNA dimerizes by forming an interstrand quadruple helix stabilized by guanine (and/or purine)-base tetrads in analogy to the well-known dimerization of telomeric DNA. We speculate that this structure may also mediate the association of genomic HIV-1 RNA in vivo, revealing how RNA itself can achieve the self-recognition required for subsequent genetic recombination.</description><subject>AIDS/HIV</subject><subject>Base Sequence</subject><subject>Biochemistry</subject><subject>Biological and medical sciences</subject><subject>Cations</subject><subject>Dimerization</subject><subject>Dimers</subject><subject>DNA</subject><subject>DNA, Viral - genetics</subject><subject>Drug Stability</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Genetics</subject><subject>Genome, Viral</subject><subject>Genomics</subject><subject>HIV</subject><subject>HIV 1</subject><subject>HIV-1 - genetics</subject><subject>HIV-1 - metabolism</subject><subject>Human immunodeficiency virus</subject><subject>human immunodeficiency virus 1</subject><subject>Hydrogen Bonding</subject><subject>Macromolecular Substances</subject><subject>Microbiology</subject><subject>Models, Structural</subject><subject>Molecular Sequence Data</subject><subject>Monovalent cations</subject><subject>Nucleic Acid Conformation</subject><subject>Nucleic acids</subject><subject>Oligodeoxyribonucleotides</subject><subject>Polymerase Chain Reaction - methods</subject><subject>Restriction Mapping</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Antisense - genetics</subject><subject>RNA, Viral - chemistry</subject><subject>RNA, Viral - genetics</subject><subject>RNA, Viral - metabolism</subject><subject>Telomere - physiology</subject><subject>Thermal stability</subject><subject>Thermodynamics</subject><subject>Transcription, Genetic</subject><subject>Virology</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1993</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUtv1DAUhS0EKkNhywokC6HuEvxI_JDYVKWPkSoQCNhanuSGepTYUzupWn49jmYYDSxgYVn2-e7xvT4IvaSkpETydxtvU6lJqUrONX-EFpRoWohKk8doQQiThapY9RQ9S2lNCNG1IkfoSFWyJkouUDi_cy34BnAXIl76EWIao_Ut_jzZNk6bHu7xRYiDHV3w2Hk83gD-4AaI7uf2LnT4ahqsx8thmHxooXONy5YP-LuLU8IUX4IPg2vwl4-nz9GTzvYJXuz2Y_Tt4vzr2VVx_elyeXZ6XTSCkrGQwEBSAGFpLduuo8xqpeiqFSvQecl8YEpWjGqmGFFVY2tlV1roVdcSYPwYvd_6bqbVAG0DPk_Vm010g40PJlhn_lS8uzE_wp2pBCcil5_symO4nSCNZnCpgb63HsKUjKyFllyo_4JUVEJpSTP45i9wHabo8x8YRuhsxesMlVuoiSGlCN2-YUrMHLeZ4zaaGGXmuHPB68Mx9_gu36y_3ek2NbbvcrKNS3ssU5IwdmAz2_9WD585-ZduuqnvR7gfM_hqC67TGOKeZFzQ3BD_Bcwb1SA</recordid><startdate>19930415</startdate><enddate>19930415</enddate><creator>Sundquist, Wesley I.</creator><creator>Heaphy, Shaun</creator><general>National Academy of Sciences of the United States of America</general><general>National Acad Sciences</general><general>National Academy of Sciences</general><scope>IQODW</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19930415</creationdate><title>Evidence for Interstrand Quadruplex Formation in the Dimerization of Human Immunodeficiency Virus 1 Genomic RNA</title><author>Sundquist, Wesley I. ; Heaphy, Shaun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c610t-7e2e71ee6a157dff12a9881bd6be96be78812874219282084ca58ab969bfd0e23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1993</creationdate><topic>AIDS/HIV</topic><topic>Base Sequence</topic><topic>Biochemistry</topic><topic>Biological and medical sciences</topic><topic>Cations</topic><topic>Dimerization</topic><topic>Dimers</topic><topic>DNA</topic><topic>DNA, Viral - genetics</topic><topic>Drug Stability</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Genetics</topic><topic>Genome, Viral</topic><topic>Genomics</topic><topic>HIV</topic><topic>HIV 1</topic><topic>HIV-1 - genetics</topic><topic>HIV-1 - metabolism</topic><topic>Human immunodeficiency virus</topic><topic>human immunodeficiency virus 1</topic><topic>Hydrogen Bonding</topic><topic>Macromolecular Substances</topic><topic>Microbiology</topic><topic>Models, Structural</topic><topic>Molecular Sequence Data</topic><topic>Monovalent cations</topic><topic>Nucleic Acid Conformation</topic><topic>Nucleic acids</topic><topic>Oligodeoxyribonucleotides</topic><topic>Polymerase Chain Reaction - methods</topic><topic>Restriction Mapping</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA, Antisense - genetics</topic><topic>RNA, Viral - chemistry</topic><topic>RNA, Viral - genetics</topic><topic>RNA, Viral - metabolism</topic><topic>Telomere - physiology</topic><topic>Thermal stability</topic><topic>Thermodynamics</topic><topic>Transcription, Genetic</topic><topic>Virology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sundquist, Wesley I.</creatorcontrib><creatorcontrib>Heaphy, Shaun</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</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>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sundquist, Wesley I.</au><au>Heaphy, Shaun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evidence for Interstrand Quadruplex Formation in the Dimerization of Human Immunodeficiency Virus 1 Genomic RNA</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>1993-04-15</date><risdate>1993</risdate><volume>90</volume><issue>8</issue><spage>3393</spage><epage>3397</epage><pages>3393-3397</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><coden>PNASA6</coden><abstract>Retroviruses package two homologous single-stranded RNA genomes within a gag protein-RNA complex. In mature virion particles, the two RNA strands are thought to associate primarily through direct RNA-RNA interactions, although the structural basis for this stable association is unknown. We now report that a 127-nucleotide (nt) HIV-1NL4-3RNA fragment (positions 732-858) encompassing the 5' end of the gag gene dimerizes spontaneously under high ionic strength conditions in the absence of any protein cofactor. The HIV-1 RNA dimer is dramatically and specifically stabilized by the monovalent cation potassium. Thermal dissociation of the dimer occurs at 80⚬C in 100 mM K+(5 mM Mg2+) but at significantly lower temperatures in the presence of either smaller or larger monovalent cations (100 mM Li+, 40⚬C; 100 mM Na+, 55⚬C; 100 mM Cs+, 30⚬C). Deletion analyses of the 3' end of the 127-nt fragment reveal that an HIV-1 RNA fragment as short as 94 nt (732-825) can dimerize spontaneously, but a further 9-base deletion of the purine-rich sequence, GGGGGAGAA from positions 817 through 825, eliminates dimerization. These experimental results support a model in which HIV-1 RNA dimerizes by forming an interstrand quadruple helix stabilized by guanine (and/or purine)-base tetrads in analogy to the well-known dimerization of telomeric DNA. We speculate that this structure may also mediate the association of genomic HIV-1 RNA in vivo, revealing how RNA itself can achieve the self-recognition required for subsequent genetic recombination.</abstract><cop>Washington, DC</cop><pub>National Academy of Sciences of the United States of America</pub><pmid>8475087</pmid><doi>10.1073/pnas.90.8.3393</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
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subjects | AIDS/HIV Base Sequence Biochemistry Biological and medical sciences Cations Dimerization Dimers DNA DNA, Viral - genetics Drug Stability Fundamental and applied biological sciences. Psychology Genetics Genome, Viral Genomics HIV HIV 1 HIV-1 - genetics HIV-1 - metabolism Human immunodeficiency virus human immunodeficiency virus 1 Hydrogen Bonding Macromolecular Substances Microbiology Models, Structural Molecular Sequence Data Monovalent cations Nucleic Acid Conformation Nucleic acids Oligodeoxyribonucleotides Polymerase Chain Reaction - methods Restriction Mapping Ribonucleic acid RNA RNA, Antisense - genetics RNA, Viral - chemistry RNA, Viral - genetics RNA, Viral - metabolism Telomere - physiology Thermal stability Thermodynamics Transcription, Genetic Virology |
title | Evidence for Interstrand Quadruplex Formation in the Dimerization of Human Immunodeficiency Virus 1 Genomic RNA |
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