{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T14:33:30Z","timestamp":1790174010814,"version":"4.1.0"},"reference-count":74,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2021,11,29]],"date-time":"2021-11-29T00:00:00Z","timestamp":1638144000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Biochemical Society","award":["Eric Reid Fund for Methodology"],"award-info":[{"award-number":["Eric Reid Fund for Methodology"]}]},{"DOI":"10.13039\/501100000265","name":"Medical Research Council","doi-asserted-by":"publisher","award":["MR\/N022939\/1"],"award-info":[{"award-number":["MR\/N022939\/1"]}],"id":[{"id":"10.13039\/501100000265","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000272","name":"National Institute for Health Research","doi-asserted-by":"publisher","award":["Cambridge BRC RCAG\/18"],"award-info":[{"award-number":["Cambridge BRC RCAG\/18"]}],"id":[{"id":"10.13039\/501100000272","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001459","name":"Ministry of Education","doi-asserted-by":"publisher","award":["Research Centres of Excellence Initiative"],"award-info":[{"award-number":["Research Centres of Excellence Initiative"]}],"id":[{"id":"10.13039\/501100001459","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>HIV-1 packages two copies of its gRNA into virions via an interaction with the viral structural protein Gag. Both copies and their native RNA structure are essential for virion infectivity. The precise stepwise nature of the packaging process has not been resolved. This is largely due to a prior lack of structural techniques that follow RNA structural changes within an RNA\u2013protein complex. Here, we apply the in-gel SHAPE (selective 2\u2019OH acylation analysed by primer extension) technique to study the initiation of HIV-1 packaging, examining the interaction between the packaging signal RNA and the Gag polyprotein, and compare it with that of the NC domain of Gag alone. Our results imply interactions between Gag and monomeric packaging signal RNA in switching the RNA conformation into a dimerisation-competent structure, and show that the Gag\u2013dimer complex then continues to stabilise. These data provide a novel insight into how HIV-1 regulates the translation and packaging of its genome.<\/jats:p>","DOI":"10.3390\/v13122389","type":"journal-article","created":{"date-parts":[[2021,12,1]],"date-time":"2021-12-01T03:12:56Z","timestamp":1638328376000},"page":"2389","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["HIV-1 Packaging Visualised by In-Gel SHAPE"],"prefix":"10.3390","volume":"13","author":[{"given":"Aaron R.","family":"D\u2019Souza","sequence":"first","affiliation":[{"name":"Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore"},{"name":"Cancer Science Institute of Singapore, National University of Singapore, Singapore 117599, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dhivya","family":"Jayaraman","sequence":"additional","affiliation":[{"name":"Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4666-9936","authenticated-orcid":false,"given":"Ziqi","family":"Long","sequence":"additional","affiliation":[{"name":"Department of Medicine, University of Cambridge, Level 5 Addenbrookes Hospital, Cambridge CB2 0QQ, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9802-6019","authenticated-orcid":false,"given":"Jingwei","family":"Zeng","sequence":"additional","affiliation":[{"name":"Department of Medicine, University of Cambridge, Level 5 Addenbrookes Hospital, Cambridge CB2 0QQ, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liam J.","family":"Prestwood","sequence":"additional","affiliation":[{"name":"Department of Medicine, University of Cambridge, Level 5 Addenbrookes Hospital, Cambridge CB2 0QQ, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charlene","family":"Chan","sequence":"additional","affiliation":[{"name":"Cancer Science Institute of Singapore, National University of Singapore, Singapore 117599, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3582-2253","authenticated-orcid":false,"given":"Dennis","family":"Kappei","sequence":"additional","affiliation":[{"name":"Cancer Science Institute of Singapore, National University of Singapore, Singapore 117599, Singapore"},{"name":"Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 117596, Singapore"},{"name":"NUS Center for Cancer Research, Yong Loo Lin School of Medicine, National University of Singapore, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew M. L.","family":"Lever","sequence":"additional","affiliation":[{"name":"Department of Medicine, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore"},{"name":"Cancer Science Institute of Singapore, National University of Singapore, Singapore 117599, Singapore"},{"name":"Department of Medicine, University of Cambridge, Level 5 Addenbrookes Hospital, Cambridge CB2 0QQ, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6055-7052","authenticated-orcid":false,"given":"Julia C.","family":"Kenyon","sequence":"additional","affiliation":[{"name":"Cancer Science Institute of Singapore, National University of Singapore, Singapore 117599, Singapore"},{"name":"Department of Medicine, University of Cambridge, Level 5 Addenbrookes Hospital, Cambridge CB2 0QQ, UK"},{"name":"Department of Microbiology and Immunology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 117545, Singapore"},{"name":"Homerton College, University of Cambridge, Cambridge CB2 8PH, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,11,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1006\/viro.1998.9398","article-title":"HIV-1 Gag Proteins: Diverse Functions in the Virus Life Cycle","volume":"251","author":"Freed","year":"1998","journal-title":"Virology"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"15005","DOI":"10.1074\/jbc.270.25.15005","article-title":"Influence of Human Immunodeficiency Virus Nucleocapsid Protein on Synthesis and Strand Transfer by the Reverse Transcriptase In Vitro","volume":"270","author":"Tsuchihashi","year":"1995","journal-title":"J. Biol. Chem."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3907","DOI":"10.1128\/JVI.72.5.3907-3915.1998","article-title":"The Role of Nucleocapsid and U5 Stem\/A-Rich Loop Sequences in TRNA3Lys Genomic Placement and Initiation of Reverse Transcription in Human Immunodeficiency Virus Type 1","volume":"72","author":"Huang","year":"1998","journal-title":"J. Virol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"4485","DOI":"10.1128\/JVI.73.5.4485-4488.1999","article-title":"The Role of Pr55gag in the Annealing of TRNA3Lys to Human Immunodeficiency Virus Type 1 Genomic RNA","volume":"73","author":"Cen","year":"1999","journal-title":"J. Virol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"4251","DOI":"10.1128\/JVI.73.5.4251-4256.1999","article-title":"The Human Immunodeficiency Virus Type 1 Gag Polyprotein Has Nucleic Acid Chaperone Activity: Possible Role in Dimerization of Genomic RNA and Placement of TRNA on the Primer Binding Site","volume":"73","author":"Feng","year":"1999","journal-title":"J. Virol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1006\/jmbi.2001.5021","article-title":"HIV-1 Nucleocapsid Protein Zinc Finger Structures Induce TRNALys, 3 Structural Changes but Are Not Critical for Primer\/Template Annealing11Edited by M. F. Summers","volume":"312","author":"Hargittai","year":"2001","journal-title":"J. Mol. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1016\/j.jmb.2004.01.054","article-title":"Mechanistic Insights into the Kinetics of HIV-1 Nucleocapsid Protein-Facilitated TRNA Annealing to the Primer Binding Site","volume":"337","author":"Hargittai","year":"2004","journal-title":"J. Mol. Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"47725","DOI":"10.1074\/jbc.M105124200","article-title":"HIV-1 Nucleocapsid Protein and the Secondary Structure of the Binary Complex Formed between TRNALys.3 and Viral RNA Template Play Different Roles during Initiation of (\u2212) Strand DNA Reverse Transcription","volume":"276","author":"Rong","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1186\/s12977-018-0407-4","article-title":"An RNA-Binding Compound That Stabilizes the HIV-1 GRNA Packaging Signal Structure and Specifically Blocks HIV-1 RNA Encapsidation","volume":"15","author":"Ingemarsdotter","year":"2018","journal-title":"Retrovirology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2557","DOI":"10.1128\/JVI.75.6.2557-2565.2001","article-title":"Duplication of the Primary Encapsidation and Dimer Linkage Region of Human Immunodeficiency Virus Type 1 RNA Results in the Appearance of Monomeric RNA in Virions","volume":"75","author":"Sakuragi","year":"2001","journal-title":"J. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Nikolaitchik, O.A., Dilley, K.A., Fu, W., Gorelick, R.J., Tai, S.-H.S., Soheilian, F., Ptak, R.G., Nagashima, K., Pathak, V.K., and Hu, W.-S. (2013). Dimeric RNA Recognition Regulates HIV-1 Genome Packaging. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003249"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1016\/j.virol.2014.01.019","article-title":"Life of Psi: How Full-Length HIV-1 RNAs Become Packaged Genomes in the Viral Particles","volume":"454\u2013455","author":"Kuzembayeva","year":"2014","journal-title":"Virology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1016\/j.tim.2019.04.003","article-title":"RNA Packaging in HIV","volume":"27","author":"Rein","year":"2019","journal-title":"Trends Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0079-6603(08)60359-1","article-title":"Structure and Function of the Human Immunodeficiency Virus Leader RNA","volume":"54","author":"Berkhout","year":"1996","journal-title":"Prog. Nucleic Acid Res. Mol. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1126\/science.1210460","article-title":"NMR Detection of Structures in the HIV-1 5\u2032-Leader RNA That Regulate Genome Packaging","volume":"334","author":"Lu","year":"2011","journal-title":"Science"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"19967","DOI":"10.1074\/jbc.M200950200","article-title":"In Vitro Evidence That the Untranslated Leader of the HIV-1 Genome Is an RNA Checkpoint That Regulates Multiple Functions through Conformational Changes","volume":"277","author":"Berkhout","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"27486","DOI":"10.1016\/S0021-9258(18)47011-1","article-title":"Mutational Analysis of the Bipartite Dimer Linkage Structure of Human Immunodeficiency Virus Type 1 Genomic RNA","volume":"269","author":"Paillart","year":"1994","journal-title":"J. Biol. Chem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1016\/S0300-9084(96)80010-1","article-title":"Dimerization of Retroviral Genomic RNAs: Structural and Functional Implications","volume":"78","author":"Paillart","year":"1996","journal-title":"Biochimie"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"5572","DOI":"10.1073\/pnas.93.11.5572","article-title":"A Loop-Loop \u201cKissing\u201d Complex Is the Essential Part of the Dimer Linkage of Genomic HIV-1 RNA","volume":"93","author":"Paillart","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/0031-6865(95)00048-8","article-title":"The Use of Chemical Modification Interference and Inverse PCR Mutagenesis to Identify the Dimerization Initiation Site of HIV-1 Genomic RNA","volume":"71","author":"Paillairt","year":"1996","journal-title":"Pharm. Acta Helv."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"4945","DOI":"10.1073\/pnas.91.11.4945","article-title":"Identification of the Primary Site of the Human Immunodeficiency Virus Type 1 RNA Dimerization In Vitro","volume":"91","author":"Skripkin","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"35061","DOI":"10.1074\/jbc.M114.621425","article-title":"A Short Sequence Motif in the 5\u2032 Leader of the HIV-1 Genome Modulates Extended RNA Dimer Formation and Virus Replication","volume":"289","author":"Das","year":"2014","journal-title":"J. Biol. Chem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4085","DOI":"10.1128\/jvi.63.9.4085-4087.1989","article-title":"Identification of a Sequence Required for Efficient Packaging of Human Immunodeficiency Virus Type 1 RNA into Virions","volume":"63","author":"Lever","year":"1989","journal-title":"J. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1038\/nrmicro1210","article-title":"How Retroviruses Select Their Genomes","volume":"3","author":"Summers","year":"2005","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"9269","DOI":"10.1021\/bi401270d","article-title":"Targeting RNA-Protein Interactions within the Human Immunodeficiency Virus Type 1 Lifecycle","volume":"52","author":"Bell","year":"2013","journal-title":"Biochemistry"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2101","DOI":"10.1128\/jvi.69.4.2101-2109.1995","article-title":"RNA Secondary Structure and Binding Sites for Gag Gene Products in the 5\u2032 Packaging Signal of Human Immunodeficiency Virus Type 1","volume":"69","author":"Clever","year":"1995","journal-title":"J. Virol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"11601","DOI":"10.1074\/jbc.M210291200","article-title":"A Novel Long Distance Base-Pairing Interaction in Human Immunodeficiency Virus Type 1 RNA Occludes the Gag Start Codon","volume":"278","author":"Abbink","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Mailler, E., Bernacchi, S., Marquet, R., Paillart, J.-C., Vivet-Boudou, V., and Smyth, R.P. (2016). The Life-Cycle of the HIV-1 Gag\u2013RNA Complex. Viruses, 8.","DOI":"10.3390\/v8090248"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1017\/S1355838201001881","article-title":"Two Alternating Structures of the HIV-1 Leader RNA","volume":"7","author":"Huthoff","year":"2001","journal-title":"RNA"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"9058","DOI":"10.1021\/bi0502588","article-title":"The HIV-1 Leader RNA Conformational Switch Regulates RNA Dimerization but Does Not Regulate MRNA Translation","volume":"44","author":"Abbink","year":"2005","journal-title":"Biochemistry"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e174","DOI":"10.1093\/nar\/gkt690","article-title":"In-Gel Probing of Individual RNA Conformers within a Mixed Population Reveals a Dimerization Structural Switch in the HIV-1 Leader","volume":"41","author":"Kenyon","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"17680","DOI":"10.1038\/srep17680","article-title":"Fate of HIV-1 CDNA Intermediates during Reverse Transcription Is Dictated by Transcription Initiation Site of Virus Genomic RNA","volume":"5","author":"Masuda","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"13378","DOI":"10.1073\/pnas.1616627113","article-title":"Transcriptional Start Site Heterogeneity Modulates the Structure and Function of the HIV-1 Genome","volume":"113","author":"Kharytonchyk","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1126\/science.aaz7959","article-title":"Structural Basis for Transcriptional Start Site Control of HIV-1 RNA Fate","volume":"368","author":"Brown","year":"2020","journal-title":"Science"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1038\/nature06998","article-title":"Imaging the Biogenesis of Individual HIV-1 Virions in Live Cells","volume":"454","author":"Jouvenet","year":"2008","journal-title":"Nature"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"5013","DOI":"10.1128\/jvi.68.8.5013-5018.1994","article-title":"Characterization of Human Immunodeficiency Virus Type 1 Dimeric RNA from Wild-Type and Protease-Defective Virions","volume":"68","author":"Fu","year":"1994","journal-title":"J. Virol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.virol.2010.08.013","article-title":"Formation of Immature and Mature Genomic RNA Dimers in Wild-Type and Protease-Inactive HIV-1: Differential Roles of the Gag Polyprotein, Nucleocapsid Proteins NCp15, NCp9, NCp7, and the Dimerization Initiation Site","volume":"407","author":"Jalalirad","year":"2010","journal-title":"Virology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"8209","DOI":"10.1074\/jbc.270.14.8209","article-title":"Dimerization of HIV-1Lai RNA at Low Ionic Strength an Autocomplementary Sequence in the 5\u2032 Leader Region Is Evidenced by an Antisense Oligonucleotide","volume":"270","author":"Muriaux","year":"1995","journal-title":"J. Biol. Chem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"13464","DOI":"10.1021\/bi00249a035","article-title":"A 19-Nucleotide Sequence Upstream of the 5\u2032 Major Splice Donor Is Part of the Dimerization Domain of Human Immunodeficiency Virus 1 Genomic RNA","volume":"33","author":"Laughrea","year":"1994","journal-title":"Biochemistry"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1093\/nar\/gkj458","article-title":"Nucleic Acid Binding and Chaperone Properties of HIV-1 Gag and Nucleocapsid Proteins","volume":"34","author":"Cruceanu","year":"2006","journal-title":"Nucleic Acids Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"7577","DOI":"10.1073\/pnas.93.15.7577","article-title":"HIV-1 Nucleocapsid Protein Induces \u201cMaturation\u201d of Dimeric Retroviral RNA in Vitro","volume":"93","author":"Feng","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Ivanchenko, S., Godinez, W.J., Lampe, M., Kr\u00e4usslich, H.-G., Eils, R., Rohr, K., Br\u00e4uchle, C., M\u00fcller, B., and Lamb, D.C. (2009). Dynamics of HIV-1 Assembly and Release. PLoS Pathog., 5.","DOI":"10.1371\/journal.ppat.1000652"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Kutluay, S.B., and Bieniasz, P.D. (2010). Analysis of the Initiating Events in HIV-1 Particle Assembly and Genome Packaging. PLoS Pathog., 6.","DOI":"10.1371\/journal.ppat.1001200"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"13033","DOI":"10.1073\/pnas.1614785113","article-title":"NMR Detection of Intermolecular Interaction Sites in the Dimeric 5\u2032-Leader of the HIV-1 Genome","volume":"113","author":"Keane","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"4950","DOI":"10.1128\/JVI.76.10.4950-4960.2002","article-title":"Cis-Acting Elements Important for Retroviral RNA Packaging Specificity","volume":"76","author":"Beasley","year":"2002","journal-title":"J. Virol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1111\/j.1600-0854.2005.00312.x","article-title":"HIV-1 Gag\u2013RNA Interaction Occurs at a Perinuclear\/Centrosomal Site; Analysis by Confocal Microscopy and FRET","volume":"6","author":"Poole","year":"2005","journal-title":"Traffic"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e14663","DOI":"10.7554\/eLife.14663","article-title":"Reconstitution of Selective HIV-1 RNA Packaging in Vitro by Membrane-Bound Gag Assemblies","volume":"5","author":"Carlson","year":"2016","journal-title":"eLife"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Barajas, B.C., Tanaka, M., Robinson, B.A., Phuong, D.J., Chutiraka, K., Reed, J.C., and Lingappa, J.R. (2018). Identifying the Assembly Intermediate in Which Gag First Associates with Unspliced HIV-1 RNA Suggests a Novel Model for HIV-1 RNA Packaging. PLoS Pathog., 14.","DOI":"10.1371\/journal.ppat.1006977"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"14369","DOI":"10.1038\/srep14369","article-title":"A Novel Combined RNA-Protein Interaction Analysis Distinguishes HIV-1 Gag Protein Binding Sites from Structural Change in the Viral RNA Leader","volume":"5","author":"Kenyon","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1979","DOI":"10.1261\/rna.1166808","article-title":"ShapeFinder: A Software System for High-Throughput Quantitative Analysis of Nucleic Acid Reactivity Information Resolved by Capillary Electrophoresis","volume":"14","author":"Vasa","year":"2008","journal-title":"RNA"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1006\/jmbi.1995.0555","article-title":"The Structure of the Human Immunodeficiency Virus Type-1 TAR RNA Reveals Principles of RNA Recognition by Tat Protein","volume":"253","author":"Karn","year":"1995","journal-title":"J. Mol. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"8099","DOI":"10.1128\/JVI.00488-09","article-title":"Roles of Gag and NCp7 in Facilitating TRNA(Lys)(3) Annealing to Viral RNA in Human Immunodeficiency Virus Type 1","volume":"83","author":"Guo","year":"2009","journal-title":"J. Virol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.virol.2009.06.036","article-title":"The Contribution of the Primer Activation Signal to Differences between Gag- and NCp7-Facilitated TRNA(Lys3) Annealing in HIV-1","volume":"391","author":"Saadatmand","year":"2009","journal-title":"Virology"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"754","DOI":"10.4161\/rna.7.6.14115","article-title":"Role of HIV-1 Nucleocapsid Protein in HIV-1 Reverse Transcription","volume":"7","author":"Levin","year":"2010","journal-title":"RNA Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/S0022-2836(02)00776-3","article-title":"Structure and Stability of Wild-Type and Mutant RNA Internal Loops from the SL-1 Domain of the HIV-1 Packaging Signal","volume":"322","author":"Greatorex","year":"2002","journal-title":"J. Mol. Biol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1439","DOI":"10.1016\/S0969-2126(00)80033-7","article-title":"The Crystal Structure of the Dimerization Initiation Site of Genomic HIV-1 RNA Reveals an Extended Duplex with Two Adenine Bulges","volume":"7","author":"Ennifar","year":"1999","journal-title":"Structure"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Wilkinson, K.A., Gorelick, R.J., Vasa, S.M., Guex, N., Rein, A., Mathews, D.H., Giddings, M.C., and Weeks, K.M. (2008). High-Throughput SHAPE Analysis Reveals Structures in HIV-1 Genomic RNA Strongly Conserved across Distinct Biological States. PLoS Biol., 6.","DOI":"10.1371\/journal.pbio.0060096"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"10478","DOI":"10.1128\/JVI.02596-05","article-title":"Human Immunodeficiency Virus Type 1 Gag Polyprotein Modulates Its Own Translation","volume":"80","author":"Anderson","year":"2006","journal-title":"J. Virol."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Tuffy, K.M., Maldonado, R.J.K., Chang, J., Rosenfeld, P., Cochrane, A., and Parent, L.J. (2020). HIV-1 Gag Forms Ribonucleoprotein Complexes with Unspliced Viral RNA at Transcription Sites. Viruses, 12.","DOI":"10.3390\/v12111281"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"22243","DOI":"10.1074\/jbc.M314326200","article-title":"Role of the Trans-Activation Response Element in Dimerization of HIV-1 RNA","volume":"279","author":"Andersen","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1186\/1742-4690-9-59","article-title":"Opening of the TAR Hairpin in the HIV-1 Genome Causes Aberrant RNA Dimerization and Packaging","volume":"9","author":"Das","year":"2012","journal-title":"Retrovirology"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1016\/j.cell.2014.09.057","article-title":"Global Changes in the RNA Binding Specificity of HIV-1 Gag Regulate Virion Genesis","volume":"159","author":"Kutluay","year":"2014","journal-title":"Cell"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"3667","DOI":"10.1093\/nar\/26.16.3667","article-title":"Mapping the RNA Binding Sites for Human Immunodeficiency Virus Type-1 Gag and NC Proteins within the Complete HIV-1 and -2 Untranslated Leader Regions","volume":"26","author":"Damgaard","year":"1998","journal-title":"Nucleic Acids Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1126\/science.279.5349.384","article-title":"Structure of the HIV-1 Nucleocapsid Protein Bound to the SL3 \u03a8-RNA Recognition Element","volume":"279","author":"Guzman","year":"1998","journal-title":"Science"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"4304","DOI":"10.1038\/ncomms5304","article-title":"Specific Recognition of the HIV-1 Genomic RNA by the Gag Precursor","volume":"5","author":"Smyth","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1126\/science.aaa9266","article-title":"Structure of the HIV-1 RNA Packaging Signal","volume":"348","author":"Keane","year":"2015","journal-title":"Science"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"17737","DOI":"10.1073\/pnas.2008519117","article-title":"Identification of the Initial Nucleocapsid Recognition Element in the HIV-1 RNA Packaging Signal","volume":"117","author":"Ding","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"3162","DOI":"10.1021\/bi2017969","article-title":"Comparative Structural Effects of HIV-1 Gag and Nucleocapsid Proteins in Binding to and Unwinding of the Viral RNA Packaging Signal","volume":"51","author":"Bell","year":"2012","journal-title":"Biochemistry"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1080\/15476286.2016.1256533","article-title":"HIV-1 Pr55Gag Binds Genomic and Spliced RNAs with Different Affinity and Stoichiometry","volume":"14","author":"Bernacchi","year":"2017","journal-title":"RNA Biol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1038\/nmeth.3490","article-title":"Mutational Interference Mapping Experiment (MIME) for Studying RNA Structure and Function","volume":"12","author":"Smyth","year":"2015","journal-title":"Nat. Methods"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"6061","DOI":"10.1128\/JVI.03277-13","article-title":"An Immature Retroviral RNA Genome Resembles a Kinetically Trapped Intermediate State","volume":"88","author":"Grohman","year":"2014","journal-title":"J. Virol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"3404","DOI":"10.1093\/nar\/gkq1314","article-title":"The Relationship between HIV-1 Genome RNA Dimerization, Virion Maturation and Infectivity","volume":"39","author":"Ohishi","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1834","DOI":"10.1128\/JVI.75.4.1834-1841.2001","article-title":"Maintenance of the Gag\/Gag-Pol Ratio Is Important for Human Immunodeficiency Virus Type 1 RNA Dimerization and Viral Infectivity","volume":"75","author":"Crowe","year":"2001","journal-title":"J. Virol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1084","DOI":"10.1016\/j.jmb.2007.06.010","article-title":"HIV-1 Viral RNA Is Selected in the Form of Monomers That Dimerize in a Three-Step Protease-Dependent Process; the DIS of Stem\u2013Loop 1 Initiates Viral RNA Dimerization","volume":"371","author":"Song","year":"2007","journal-title":"J. Mol. Biol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/12\/2389\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:37:20Z","timestamp":1760168240000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/12\/2389"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,29]]},"references-count":74,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["v13122389"],"URL":"https:\/\/doi.org\/10.3390\/v13122389","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,29]]}}}