The thermodynamics of Pr55Gag-RNA interaction regulate the assembly of HIV
The interactions that occur during HIV Pr55Gag oligomerization and genomic RNA packaging are essential elements that facilitate HIV assembly. However, mechanistic details of these interactions are not clearly defined. Here, we overcome previous limitations in producing large quantities of full-lengt...
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| creator | Tanwar, Hanumant S Khoo, Keith K Garvey, Megan Waddington, Lynne Leis, Andrew Hijnen, Marcel Velkov, Tony Dumsday, Geoff J McKinstry, William J Mak, Johnson |
| description | The interactions that occur during HIV Pr55Gag oligomerization and genomic RNA packaging are essential elements that facilitate HIV assembly. However, mechanistic details of these interactions are not clearly defined. Here, we overcome previous limitations in producing large quantities of full-length recombinant Pr55Gag that is required for isothermal titration calorimetry (ITC) studies, and we have revealed the thermodynamic properties of HIV assembly for the first time. Thermodynamic analysis showed that the binding between RNA and HIV Pr55Gag is an energetically favourable reaction (ΔG |
| doi_str_mv | 10.1371/journal.ppat.1006221 |
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However, mechanistic details of these interactions are not clearly defined. Here, we overcome previous limitations in producing large quantities of full-length recombinant Pr55Gag that is required for isothermal titration calorimetry (ITC) studies, and we have revealed the thermodynamic properties of HIV assembly for the first time. Thermodynamic analysis showed that the binding between RNA and HIV Pr55Gag is an energetically favourable reaction (ΔG<0) that is further enhanced by the oligomerization of Pr55Gag. The change in enthalpy (ΔH) widens sequentially from: (1) Pr55Gag-Psi RNA binding during HIV genome selection; to (2) Pr55Gag-Guanosine Uridine (GU)-containing RNA binding in cytoplasm/plasma membrane; and then to (3) Pr55Gag-Adenosine(A)-containing RNA binding in immature HIV. These data imply the stepwise increments of heat being released during HIV biogenesis may help to facilitate the process of viral assembly. By mimicking the interactions between A-containing RNA and oligomeric Pr55Gag in immature HIV, it was noted that a p6 domain truncated Pr50Gag Δp6 is less efficient than full-length Pr55Gag in this thermodynamic process. These data suggest a potential unknown role of p6 in Pr55Gag-Pr55Gag oligomerization and/or Pr55Gag-RNA interaction during HIV assembly. Our data provide direct evidence on how nucleic acid sequences and the oligomeric state of Pr55Gag regulate HIV assembly.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1006221</identifier><identifier>PMID: 28222188</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Amino Acid Sequence ; Base Sequence ; Biology and Life Sciences ; Blotting, Western ; Calorimetry ; Chromatography ; Funding ; Genomes ; HIV-1 - physiology ; Immunoprecipitation ; Laboratories ; Lentivirus ; Manufacturing ; Medicine ; Medicine and Health Sciences ; Microscopy ; Microscopy, Electron ; Physical Sciences ; Protein Precursors - chemistry ; Proteins ; Research and Analysis Methods ; Retroviridae ; RNA, Viral - chemistry ; Thermodynamics ; Virus Assembly - physiology</subject><ispartof>PLoS pathogens, 2017-02, Vol.13 (2), p.e1006221-e1006221</ispartof><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: -RNA interaction regulate the assembly of HIV. PLoS Pathog 13(2): e1006221. doi:10.1371/journal.ppat.1006221</rights><rights>2017 Tanwar et al 2017 Tanwar et al</rights><rights>2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: -RNA interaction regulate the assembly of HIV. PLoS Pathog 13(2): e1006221. doi:10.1371/journal.ppat.1006221</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c489t-1dea7296fabda9c6fe967dcc60d5450bce11662b707d05125015d8ce9bde0d2a3</citedby><cites>FETCH-LOGICAL-c489t-1dea7296fabda9c6fe967dcc60d5450bce11662b707d05125015d8ce9bde0d2a3</cites><orcidid>0000-0002-5229-5707 ; 0000-0001-7988-7334 ; 0000-0003-4905-9401 ; 0000-0002-5080-8791</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/PMC5336307/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5336307/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28222188$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tanwar, Hanumant S</creatorcontrib><creatorcontrib>Khoo, Keith K</creatorcontrib><creatorcontrib>Garvey, Megan</creatorcontrib><creatorcontrib>Waddington, Lynne</creatorcontrib><creatorcontrib>Leis, Andrew</creatorcontrib><creatorcontrib>Hijnen, Marcel</creatorcontrib><creatorcontrib>Velkov, Tony</creatorcontrib><creatorcontrib>Dumsday, Geoff J</creatorcontrib><creatorcontrib>McKinstry, William J</creatorcontrib><creatorcontrib>Mak, Johnson</creatorcontrib><title>The thermodynamics of Pr55Gag-RNA interaction regulate the assembly of HIV</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>The interactions that occur during HIV Pr55Gag oligomerization and genomic RNA packaging are essential elements that facilitate HIV assembly. However, mechanistic details of these interactions are not clearly defined. Here, we overcome previous limitations in producing large quantities of full-length recombinant Pr55Gag that is required for isothermal titration calorimetry (ITC) studies, and we have revealed the thermodynamic properties of HIV assembly for the first time. Thermodynamic analysis showed that the binding between RNA and HIV Pr55Gag is an energetically favourable reaction (ΔG<0) that is further enhanced by the oligomerization of Pr55Gag. The change in enthalpy (ΔH) widens sequentially from: (1) Pr55Gag-Psi RNA binding during HIV genome selection; to (2) Pr55Gag-Guanosine Uridine (GU)-containing RNA binding in cytoplasm/plasma membrane; and then to (3) Pr55Gag-Adenosine(A)-containing RNA binding in immature HIV. These data imply the stepwise increments of heat being released during HIV biogenesis may help to facilitate the process of viral assembly. By mimicking the interactions between A-containing RNA and oligomeric Pr55Gag in immature HIV, it was noted that a p6 domain truncated Pr50Gag Δp6 is less efficient than full-length Pr55Gag in this thermodynamic process. These data suggest a potential unknown role of p6 in Pr55Gag-Pr55Gag oligomerization and/or Pr55Gag-RNA interaction during HIV assembly. Our data provide direct evidence on how nucleic acid sequences and the oligomeric state of Pr55Gag regulate HIV assembly.</description><subject>Acids</subject><subject>Amino Acid Sequence</subject><subject>Base Sequence</subject><subject>Biology and Life Sciences</subject><subject>Blotting, Western</subject><subject>Calorimetry</subject><subject>Chromatography</subject><subject>Funding</subject><subject>Genomes</subject><subject>HIV-1 - physiology</subject><subject>Immunoprecipitation</subject><subject>Laboratories</subject><subject>Lentivirus</subject><subject>Manufacturing</subject><subject>Medicine</subject><subject>Medicine and Health Sciences</subject><subject>Microscopy</subject><subject>Microscopy, Electron</subject><subject>Physical Sciences</subject><subject>Protein Precursors - chemistry</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Retroviridae</subject><subject>RNA, Viral - chemistry</subject><subject>Thermodynamics</subject><subject>Virus Assembly - 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Academic</collection><collection>Nucleic Acids Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tanwar, Hanumant S</au><au>Khoo, Keith K</au><au>Garvey, Megan</au><au>Waddington, Lynne</au><au>Leis, Andrew</au><au>Hijnen, Marcel</au><au>Velkov, Tony</au><au>Dumsday, Geoff J</au><au>McKinstry, William J</au><au>Mak, Johnson</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The thermodynamics of Pr55Gag-RNA interaction regulate the assembly of HIV</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2017-02-01</date><risdate>2017</risdate><volume>13</volume><issue>2</issue><spage>e1006221</spage><epage>e1006221</epage><pages>e1006221-e1006221</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>The interactions that occur during HIV Pr55Gag oligomerization and genomic RNA packaging are essential elements that facilitate HIV assembly. However, mechanistic details of these interactions are not clearly defined. Here, we overcome previous limitations in producing large quantities of full-length recombinant Pr55Gag that is required for isothermal titration calorimetry (ITC) studies, and we have revealed the thermodynamic properties of HIV assembly for the first time. Thermodynamic analysis showed that the binding between RNA and HIV Pr55Gag is an energetically favourable reaction (ΔG<0) that is further enhanced by the oligomerization of Pr55Gag. The change in enthalpy (ΔH) widens sequentially from: (1) Pr55Gag-Psi RNA binding during HIV genome selection; to (2) Pr55Gag-Guanosine Uridine (GU)-containing RNA binding in cytoplasm/plasma membrane; and then to (3) Pr55Gag-Adenosine(A)-containing RNA binding in immature HIV. These data imply the stepwise increments of heat being released during HIV biogenesis may help to facilitate the process of viral assembly. By mimicking the interactions between A-containing RNA and oligomeric Pr55Gag in immature HIV, it was noted that a p6 domain truncated Pr50Gag Δp6 is less efficient than full-length Pr55Gag in this thermodynamic process. These data suggest a potential unknown role of p6 in Pr55Gag-Pr55Gag oligomerization and/or Pr55Gag-RNA interaction during HIV assembly. Our data provide direct evidence on how nucleic acid sequences and the oligomeric state of Pr55Gag regulate HIV assembly.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28222188</pmid><doi>10.1371/journal.ppat.1006221</doi><orcidid>https://orcid.org/0000-0002-5229-5707</orcidid><orcidid>https://orcid.org/0000-0001-7988-7334</orcidid><orcidid>https://orcid.org/0000-0003-4905-9401</orcidid><orcidid>https://orcid.org/0000-0002-5080-8791</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Acids Amino Acid Sequence Base Sequence Biology and Life Sciences Blotting, Western Calorimetry Chromatography Funding Genomes HIV-1 - physiology Immunoprecipitation Laboratories Lentivirus Manufacturing Medicine Medicine and Health Sciences Microscopy Microscopy, Electron Physical Sciences Protein Precursors - chemistry Proteins Research and Analysis Methods Retroviridae RNA, Viral - chemistry Thermodynamics Virus Assembly - physiology |
| title | The thermodynamics of Pr55Gag-RNA interaction regulate the assembly of HIV |
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