Structural maturation of the HIV-1 RNA 5’ untranslated region by Pr55^Gag and its maturation products

References

• Swanstrom R, Wills JW. Synthesis, assembly, and processing of viral proteins [Internet]. In: Coffin JM, Hughes SH, and Varmus HE, editors. Retroviruses. Cold Spring Harbor (NY):Cold Spring Harbor Laboratory Press; 1997. Available from: http://www.ncbi.nlm.nih.gov/books/NBK19456/
   Google Scholar
• Sundquist WI, Kräusslich H-G. HIV-1 assembly, budding, and maturation. Cold Spring Harb Perspect Med. 2012;2:a006924.
   PubMed Web of Science ®Google Scholar
• Freed EO. HIV-1 assembly, release and maturation. Nat Rev Microbiol. 2015;13:484–496.
   PubMed Web of Science ®Google Scholar
• Kleinpeter AB, Freed EO. HIV-1 maturation: lessons learned from inhibitors. Viruses. 2020;12(9):940. https://doi.org/10.3390/v12090940
   PubMed Web of Science ®Google Scholar
• Fu W, Gorelick RJ, Rein A. Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and protease-defective virions. J Virol. 1994;68:5013–5018.
   PubMed Web of Science ®Google Scholar
• Jalalirad M, Laughrea M. 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. Virology. 2010;407:225–236.
   PubMed Web of Science ®Google Scholar
• Lee S-K, Potempa M, Kolli M, et al. Context surrounding processing sites is crucial in determining cleavage rate of a subset of processing sites in HIV-1 Gag and Gag-Pro-Pol polyprotein precursors by viral protease. J Biol Chem. 2012;287:13279–13290.
   PubMed Web of Science ®Google Scholar
• Potempa M, Nalivaika E, Ragland D, et al. A direct interaction with RNA dramatically enhances the catalytic activity of the HIV-1 protease in vitro. J Mol Biol. 2015;427:2360–2378.
   PubMed Web of Science ®Google Scholar
• Schur FKM, Hagen WJH, Rumlová M, et al. Structure of the immature HIV-1 capsid in intact virus particles at 8.8 Å resolution. Nature. 2015;517(7535):505–8. https://doi.org/10.1038/nature13838
   PubMed Web of Science ®Google Scholar
• Mattei S, Glass B, Hagen WJH, et al. The structure and flexibility of conical HIV-1 capsids determined within intact virions. Science. 2016;354(6318):1434–1437.
   PubMed Web of Science ®Google Scholar
• Mattei S, Tan A, Glass B, et al. High-resolution structures of HIV-1 Gag cleavage mutants determine structural switch for virus maturation. Proc Natl Acad Sci USA. 2018;115:E9401–10.
   PubMed Web of Science ®Google Scholar
• Shehu-Xhilaga M, Kraeusslich HG, Pettit S, et al. Proteolytic processing of the p2/nucleocapsid cleavage site is critical for human immunodeficiency virus type 1 RNA dimer maturation. J Virol. 2001;75:9156–9164.
   PubMed Web of Science ®Google Scholar
• Wu T, Datta SAK, Mitra M, et al. Fundamental differences between the nucleic acid chaperone activities of HIV-1 nucleocapsid protein and Gag or Gag-derived proteins: biological implications. Virology. 2010;405:556–567.
   PubMed Web of Science ®Google Scholar
• Darlix J-L, de Rocquigny H, Mély Y. The multiple roles of the nucleocapsid in retroviral RNA conversion into proviral DNA by reverse transcriptase. Biochem Soc Trans. 2016;44:1427–1440.
   PubMed Web of Science ®Google Scholar
• Levin JG, Guo J, Rouzina I, et al. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog Nucleic Acid Res Mol Biol. 2005;80:217–286.
   PubMed Web of Science ®Google Scholar
• Feng YX, Copeland TD, Henderson LE, et al. HIV-1 nucleocapsid protein induces “maturation” of dimeric retroviral RNA in vitro. Proc Natl Acad Sci USA. 1996;93:7577–7581.
   PubMed Web of Science ®Google Scholar
• Müller B, Anders M, Akiyama H, et al. HIV-1 Gag processing intermediates trans-dominantly interfere with HIV-1 infectivity. J Biol Chem. 2009;284:29692–29703.
   PubMed Web of Science ®Google Scholar
• Wiegers K, Rutter G, Kottler H, et al. Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J Virol. 1998;72:2846–2854.
   PubMed Web of Science ®Google Scholar
• Ohishi M, Nakano T, Sakuragi S, et al. The relationship between HIV-1 genome RNA dimerization, virion maturation and infectivity. Nucleic Acids Res. 2011;39:3404–3417.
   PubMed Web of Science ®Google Scholar
• Song R, Kafaie J, Yang L, et al. HIV-1 viral RNA is selected in the form of monomers that dimerize in a three-step protease-dependent process; the DIS of stem-loop 1 initiates viral RNA dimerization. J Mol Biol. 2007;371:1084–1098.
   PubMed Web of Science ®Google Scholar
• Mattei S, Flemming A, Anders-Össwein M, et al. RNA and nucleocapsid are dispensable for mature HIV-1 capsid assembly. J Virol. 2015;89:9739–9747.
   PubMed Web of Science ®Google Scholar
• Kräusslich HG, Fäcke M, Heuser AM, et al. The spacer peptide between human immunodeficiency virus capsid and nucleocapsid proteins is essential for ordered assembly and viral infectivity. J Virol. 1995;69:3407–3419.
   PubMed Web of Science ®Google Scholar
• Berkhout B, Das AT, van Wamel JL. The native structure of the human immunodeficiency virus type 1 RNA genome is required for the first strand transfer of reverse transcription. Virology. 1998;249:211–218.
   PubMed Web of Science ®Google Scholar
• Paillart JC, Berthoux L, Ottmann M, et al. A dual role of the putative RNA dimerization initiation site of human immunodeficiency virus type 1 in genomic RNA packaging and proviral DNA synthesis. J Virol. 1996;70:8348–8354.
   PubMed Web of Science ®Google Scholar
• Lyonnais S, Sadiq SK, Lorca-Oró C, et al. The HIV-1 ribonucleoprotein dynamically regulates its condensate behavior and drives acceleration of protease activity through membrane-less granular phase-separation [Internet]. 2019. [cited 2021 Sept 23] Available from: https://www.biorxiv.org/content/10.1101/528638v2
   Google Scholar
• Wilkinson KA, Gorelick RJ, Vasa SM, et al. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol. 2008;6:e96.
   PubMed Web of Science ®Google Scholar
• Watts JM, Dang KK, Gorelick RJ, et al. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature. 2009;460:711–716.
   PubMed Web of Science ®Google Scholar
• Pirakitikulr N, Kohlway A, Lindenbach BD, et al. The coding region of the HCV genome contains a network of regulatory RNA structures. Mol Cell. 2016;62:111–120.
   PubMed Web of Science ®Google Scholar
• Manfredonia I, Nithin C, Ponce-Salvatierra A, et al. Genome-wide mapping of SARS-CoV-2 RNA structures identifies therapeutically-relevant elements. Nucleic Acids Res. 2020;48:12436–12452.
   PubMed Web of Science ®Google Scholar
• Ew AE-W, Smyth RP, Mailler E, et al. Specific recognition of the HIV-1 genomic RNA by the Gag precursor. Nat Commun. 2014;5:4304.
   PubMed Web of Science ®Google Scholar
• Kenyon JC, Prestwood LJ, Lever AML. A novel combined RNA-protein interaction analysis distinguishes HIV-1 Gag protein binding sites from structural change in the viral RNA leader. Sci Rep. 2015;5:14369.
   PubMed Web of Science ®Google Scholar
• Damgaard CK, Dyhr-Mikkelsen H, Kjems J. 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. Nucleic Acids Res. 1998;26:3667–3676.
   PubMed Web of Science ®Google Scholar
• Zeffman A, Hassard S, Varani G, et al. The major HIV-1 packaging signal is an extended bulged stem loop whose structure is altered on interaction with the Gag polyprotein. J Mol Biol. 2000;297:877–893.
   PubMed Web of Science ®Google Scholar
• Ding P, Kharytonchyk S, Waller A, et al. Identification of the initial nucleocapsid recognition element in the HIV-1 RNA packaging signal. Proc Natl Acad Sci USA. 2020;117:17737–17746.
   PubMed Web of Science ®Google Scholar
• Paillart J-C, Dettenhofer M, Yu X-F, et al. First snapshots of the HIV-1 RNA structure in infected cells and in virions. J Biol Chem. 2004;279:48397–48403.
   PubMed Web of Science ®Google Scholar
• Isel C, Ehresmann C, Keith G, et al. Initiation of reverse transcription of HIV-1: secondary structure of the HIV-1 RNA/tRNA(3Lys) (template/primer). J Mol Biol. 1995;247:236–250.
   PubMed Web of Science ®Google Scholar
• Isel C, Westhof E, Massire C, et al. Structural basis for the specificity of the initiation of HIV-1 reverse transcription. EMBO J. 1999;18:1038–1048.
   PubMed Web of Science ®Google Scholar
• Sleiman D, Goldschmidt V, Barraud P, et al. Initiation of HIV-1 reverse transcription and functional role of nucleocapsid-mediated tRNA/viral genome interactions. Virus Res. 2012;169:324–339.
   PubMed Web of Science ®Google Scholar
• Beerens N, Groot F, Berkhout B. Initiation of HIV-1 reverse transcription is regulated by a primer activation signal. J Biol Chem. 2001;276:31247–31256.
   PubMed Web of Science ®Google Scholar
• Beerens N, Berkhout B. Switching the in vitro tRNA usage of HIV-1 by simultaneous adaptation of the PBS and PAS. RNA. 2002;8:357–369.
   PubMed Web of Science ®Google Scholar
• Smyth RP, Despons L, Huili G, et al. Mutational interference mapping experiment (MIME) for studying RNA structure and function. Nat Methods. 2015;12:866–872.
   PubMed Web of Science ®Google Scholar
• Smyth RP, Smith MR, Jousset A-C, et al. In cell mutational interference mapping experiment (in cell MIME) identifies the 5ʹ polyadenylation signal as a dual regulator of HIV-1 genomic RNA production and packaging. Nucleic Acids Res. 2018;46:e57.
   PubMed Web of Science ®Google Scholar
• Lu K, Heng X, Summers MF. Structural determinants and mechanism of HIV-1 genome packaging. J Mol Biol. 2011;410:609–633.
   PubMed Web of Science ®Google Scholar
• Keane SC, Summers MF. NMR studies of the structure and function of the HIV-1 5ʹ-leader. Viruses. 2016;8(12):338. https://doi.org/10.3390/v8120338
   PubMed Web of Science ®Google Scholar
• Mailler E, Bernacchi S, Marquet R, et al. The Life-Cycle of the HIV-1 Gag-RNA complex. Viruses. 2016;8(9):248. https://doi.org/10.3390/v8090248
   PubMed Web of Science ®Google Scholar
• Harrison GP, Lever AM. The human immunodeficiency virus type 1 packaging signal and major splice donor region have a conserved stable secondary structure. J Virol. 1992;66:4144–4153.
   PubMed Web of Science ®Google Scholar
• Berkhout B. Structure and function of the human immunodeficiency virus leader RNA. Prog Nucleic Acid Res Mol Biol. 1996;54:1–34.
   PubMedGoogle Scholar
• Harrison GP, Miele G, Hunter E, et al. Functional analysis of the core human immunodeficiency virus type 1 packaging signal in a permissive cell line. J Virol. 1998;72:5886–5896.
   PubMed Web of Science ®Google Scholar
• Skripkin E, Paillart JC, Marquet R, et al. Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proc Natl Acad Sci USA. 1994;91:4945–4949.
   PubMed Web of Science ®Google Scholar
• Paillart JC, Skripkin E, Ehresmann B, et al. A loop-loop “kissing” complex is the essential part of the dimer linkage of genomic HIV-1 RNA. Proc Natl Acad Sci USA. 1996;93:5572–5577.
   PubMed Web of Science ®Google Scholar
• Merino EJ, Wilkinson KA, Coughlan JL, et al. RNA structure analysis at single nucleotide resolution by selective 2ʹ-hydroxyl acylation and primer extension (SHAPE). J Am Chem Soc. 2005;127:4223–4231.
   PubMed Web of Science ®Google Scholar
• Badorrek CS, Weeks KM. RNA flexibility in the dimerization domain of a gamma retrovirus. Nat Chem Biol. 2005;1:104–111.
   PubMed Web of Science ®Google Scholar
• Aktar SJ, Jabeen A, Ali LM, et al. SHAPE analysis of the 5ʹ end of the Mason-Pfizer monkey virus (MPMV) genomic RNA reveals structural elements required for genome dimerization. RNA. 2013;19:1648–1658.
   PubMed Web of Science ®Google Scholar
• Gherghe C, Lombo T, Leonard CW, et al. Definition of a high-affinity Gag recognition structure mediating packaging of a retroviral RNA genome. Proc Natl Acad Sci USA. 2010;107:19248–19253.
   PubMed Web of Science ®Google Scholar
• Grohman JK, Gorelick RJ, Lickwar CR, et al. A guanosine-centric mechanism for RNA chaperone function. Science. 2013;340:190–195.
   PubMed Web of Science ®Google Scholar
• Briggs JAG, Simon MN, Gross I, et al. The stoichiometry of Gag protein in HIV-1. Nat Struct Mol Biol. 2004;11:672–675.
   PubMed Web of Science ®Google Scholar
• Rein A. Retroviral RNA packaging: a review. Arch Virol Suppl. 1994;9:513–522.
   PubMedGoogle Scholar
• Bernacchi S, Abd El-Wahab EW, Dubois N, et al. HIV-1 Pr55Gag binds genomic and spliced RNAs with different affinity and stoichiometry. RNA Biol. 2017;14:90–103.
   PubMed Web of Science ®Google Scholar
• Muriaux D, Girard PM, Bonnet-Mathonière B, et al. Dimerization of HIV-1Lai RNA at low ionic strength. An autocomplementary sequence in the 5ʹ leader region is evidenced by an antisense oligonucleotide. J Biol Chem. 1995;270:8209–8216.
   PubMed Web of Science ®Google Scholar
• Laughrea M, Jetté L. Kissing-loop model of HIV-1 genome dimerization: HIV-1 RNAs can assume alternative dimeric forms, and all sequences upstream or downstream of hairpin 248-271 are dispensable for dimer formation. Biochemistry. 1996;35:1589–1598.
   PubMed Web of Science ®Google Scholar
• Seif E, Niu M, Kleiman L. In virio SHAPE analysis of tRNA(Lys3) annealing to HIV-1 genomic RNA in wild type and protease-deficient virus. Retrovirology. 2015;12:40.
   PubMed Web of Science ®Google Scholar
• Abbink TEM, Berkhout B. A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the Gag start codon. J Biol Chem. 2003;278:11601–11611.
   PubMed Web of Science ®Google Scholar
• Keane SC, Heng X, Lu K, et al. RNA structure. Structure of the HIV-1 RNA packaging signal. Science. 2015;348:917–921.
   PubMed Web of Science ®Google Scholar
• Stewart-Maynard KM, Cruceanu M, Wang F, et al. Retroviral nucleocapsid proteins display nonequivalent levels of nucleic acid chaperone activity. J Virol. 2008;82:10129–10142.
   PubMed Web of Science ®Google Scholar
• Cruceanu M, Urbaneja MA, Hixson CV, et al. Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins. Nucleic Acids Res. 2006;34:593–605.
   PubMed Web of Science ®Google Scholar
• Berkowitz RD, Ohagen A, Höglund S, et al. Retroviral nucleocapsid domains mediate the specific recognition of genomic viral RNAs by chimeric Gag polyproteins during RNA packaging in vivo. J Virol. 1995;69:6445–6456.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Barklis E. Nucleocapsid protein effects on the specificity of retrovirus RNA encapsidation. J Virol. 1995;69:5716–5722.
   PubMed Web of Science ®Google Scholar
• Dupraz P, Spahr PF. Specificity of Rous sarcoma virus nucleocapsid protein in genomic RNA packaging. J Virol. 1992;66:4662–4670.
   PubMed Web of Science ®Google Scholar
• Holmstrom ED, Liu Z, Nettels D, et al. Disordered RNA chaperones can enhance nucleic acid folding via local charge screening. Nat Commun. 2019;10:2453.
   PubMed Web of Science ®Google Scholar
• Basu S, Bahadur RP. A structural perspective of RNA recognition by intrinsically disordered proteins. Cell Mol Life Sci. 2016;73:4075–4084.
   PubMed Web of Science ®Google Scholar
• Chu T-H, Liou A-T, Su P-Y, et al. Nucleic acid chaperone activity associated with the arginine-rich domain of human hepatitis B virus core protein. J Virol. 2014;88:2530–2543.
   PubMed Web of Science ®Google Scholar
• Nikolaitchik OA, Somoulay X, Rawson JMO, et al. Unpaired guanosines in the 5ʹ untranslated region of HIV-1 RNA act synergistically to mediate genome packaging. J Virol. 2020;94.e00439–20.
   PubMed Web of Science ®Google Scholar
• Wang W, Naiyer N, Mitra M, et al. Distinct nucleic acid interaction properties of HIV-1 nucleocapsid protein precursor NCp15 explain reduced viral infectivity. Nucleic Acids Res. 2014;42:7145–7159.
   PubMed Web of Science ®Google Scholar
• Zila V, Margiotta E, Turoňová B, et al. Cone-shaped HIV-1 capsids are transported through intact nuclear pores. Cell. 2021;184:1032–1046.e18.
   PubMed Web of Science ®Google Scholar
• Li C, Burdick RC, Nagashima K, et al. HIV-1 cores retain their integrity until minutes before uncoating in the nucleus. Proc Natl Acad Sci U S A. 2021;118.e2019467118.
   Web of Science ®Google Scholar
• Larsen KP, Mathiharan YK, Kappel K, et al. Architecture of an HIV-1 reverse transcriptase initiation complex. Nature. 2018;557:118–122.
   PubMed Web of Science ®Google Scholar
• McKinstry WJ, Hijnen M, Tanwar HS, et al. Expression and purification of soluble recombinant full length HIV-1 Pr55(Gag) protein in Escherichia coli. Protein Expr Purif. 2014;100:10–18.
   PubMed Web of Science ®Google Scholar
• Lee BM, De Guzman RN, Turner BG, et al. Dynamical behavior of the HIV-1 nucleocapsid protein. J Mol Biol. 1998;279:633–649.
   PubMed Web of Science ®Google Scholar
• De Guzman RN, Wu ZR, Stalling CC, et al. Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science. 1998;279:384–388.
   PubMed Web of Science ®Google Scholar
• Mouhand A, Belfetmi A, Catala M, et al. Modulation of the HIV nucleocapsid dynamics finely tunes its RNA-binding properties during virion genesis. Nucleic Acids Res. 2018;46:9699–9710.
   PubMed Web of Science ®Google Scholar
• Sinck L, Richer D, Howard J, et al. In vitro dimerization of human immunodeficiency virus type 1 (HIV-1) spliced RNAs. RNA. 2007;13:2141–2150.
   PubMed Web of Science ®Google Scholar
• Karabiber F, McGinnis JL, Favorov OV, et al. QuShape: rapid, accurate, and best-practices quantification of nucleic acid probing information, resolved by capillary electrophoresis. RNA. 2013;19:63–73.
   PubMed Web of Science ®Google Scholar
• Smola MJ, Calabrese JM, Weeks KM. Detection of RNA-Protein interactions in living cells with SHAPE. Biochemistry. 2015;54:6867–6875.
   PubMed Web of Science ®Google Scholar
• Reuter JS, Mathews DH. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics. 2010;11:129.
   PubMed Web of Science ®Google Scholar