1m5l › Citations

Structure and stability of wild-type and mutant RNA internal loops from the SL-1 domain of the HIV-1 packaging signal.

Greatorex J, Gallego J, Varani G, Lever A
J Mol Biol 322 543-57 (2002)
Cited: 43 times
EuropePMC logo PMID: 12225748

Abstract

The packaging signal (Psi) of the human immunodeficiency virus type 1 (HIV-1) enables encapsidation of the full-length genomic RNA against a background of a vast excess of cellular mRNAs. The core HIV-1 Psi is approximately 109 nucleotides and contains sequences critical for viral genomic dimerisation and splicing, in addition to the packaging signal. It consists of a series of stem-loops (termed SL-1 to SL-4), which can be arranged in a cloverleaf secondary structure. Using a combination of NMR spectroscopy, UV melting experiments, molecular modeling and phylogenetic analyses, we have explored the structure of two conserved internal loops proximal to the palindromic sequence of SL-1. Internal loop A, composed of six purines, forms a flexible structure that is strikingly similar to the Rev responsive element motif when bound to Rev protein. This result suggests that it may function as a protein-binding site. The absolutely conserved four-purine internal loop B is instead conformationally and thermodynamically unstable, and exhibits multiple conformations in solution. By introducing a double AGG to GGA mutation within this loop, its conformation is stabilised to form a new intra-molecular G:A:G base-triplet. The structure of the GGA mutant explains the relative instability of the wild-type loop. In a manner analogous to SL-3, we propose that conformational flexibility at this site may facilitate melting of the structure during Gag protein capture or genomic RNA dimerisation.

Reviews - 1m5l mentioned but not cited (1)

  1. Structural and computational studies of HIV-1 RNA. Levintov L, Vashisth H. RNA Biol 21 1-32 (2024)

Articles - 1m5l mentioned but not cited (3)

  1. High-resolution NMR structure of an RNA model system: the 14-mer cUUCGg tetraloop hairpin RNA. Nozinovic S, Fürtig B, Jonker HR, Richter C, Schwalbe H. Nucleic Acids Res 38 683-694 (2010)
  2. Small-angle X-ray scattering-derived structure of the HIV-1 5' UTR reveals 3D tRNA mimicry. Jones CP, Cantara WA, Olson ED, Musier-Forsyth K. Proc Natl Acad Sci U S A 111 3395-3400 (2014)
  3. Systematics for types and effects of RNA variations. Vihinen M. RNA Biol 18 481-498 (2021)


Reviews citing this publication (9)

  1. Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV. Brierley I, Dos Ramos FJ. Virus Res 119 29-42 (2006)
  2. HIV-1 RNA dimerization: It takes two to tango. Moore MD, Hu WS. AIDS Rev 11 91-102 (2009)
  3. Retroviral RNA Dimerization: From Structure to Functions. Dubois N, Marquet R, Paillart JC, Bernacchi S. Front Microbiol 9 527 (2018)
  4. Rev: beyond nuclear export. Groom HCT, Anderson EC, Lever AML. J Gen Virol 90 1303-1318 (2009)
  5. The retroviral RNA dimer linkage: different structures may reflect different roles. Greatorex J. Retrovirology 1 22 (2004)
  6. Lentiviral vectors. Lever AM, Strappe PM, Zhao J. J Biomed Sci 11 439-449 (2004)
  7. HIV-1 replication and the cellular eukaryotic translation apparatus. Guerrero S, Batisse J, Libre C, Bernacchi S, Marquet R, Paillart JC. Viruses 7 199-218 (2015)
  8. NMR Studies of Retroviral Genome Packaging. Boyd PS, Brown JB, Brown JD, Catazaro J, Chaudry I, Ding P, Dong X, Marchant J, O'Hern CT, Singh K, Swanson C, Summers MF, Yasin S. Viruses 12 E1115 (2020)
  9. Evaluating RNA Structural Flexibility: Viruses Lead the Way. Fairman CW, Lever AML, Kenyon JC. Viruses 13 2130 (2021)

Articles citing this publication (30)

  1. First snapshots of the HIV-1 RNA structure in infected cells and in virions. Paillart JC, Dettenhofer M, Yu XF, Ehresmann C, Ehresmann B, Marquet R. J Biol Chem 279 48397-48403 (2004)
  2. Integrated self-inactivating lentiviral vectors produce full-length genomic transcripts competent for encapsidation and integration. Logan AC, Haas DL, Kafri T, Kohn DB. J Virol 78 8421-8436 (2004)
  3. DDX1 is an RNA-dependent ATPase involved in HIV-1 Rev function and virus replication. Edgcomb SP, Carmel AB, Naji S, Ambrus-Aikelin G, Reyes JR, Saphire AC, Gerace L, Williamson JR. J Mol Biol 415 61-74 (2012)
  4. Structure of the intact stem and bulge of HIV-1 Psi-RNA stem-loop SL1. Lawrence DC, Stover CC, Noznitsky J, Wu Z, Summers MF. J Mol Biol 326 529-542 (2003)
  5. Translational regulation of HIV-1 replication by HIV-1 Rev cellular cofactors Sam68, eIF5A, hRIP, and DDX3. Liu J, Henao-Mejia J, Liu H, Zhao Y, He JJ. J Neuroimmune Pharmacol 6 308-321 (2011)
  6. Structure of the RNA signal essential for translational frameshifting in HIV-1. Gaudin C, Mazauric MH, Traïkia M, Guittet E, Yoshizawa S, Fourmy D. J Mol Biol 349 1024-1035 (2005)
  7. In-gel probing of individual RNA conformers within a mixed population reveals a dimerization structural switch in the HIV-1 leader. Kenyon JC, Prestwood LJ, Le Grice SF, Lever AM. Nucleic Acids Res 41 e174 (2013)
  8. Solution RNA structures of the HIV-1 dimerization initiation site in the kissing-loop and extended-duplex dimers. Baba S, Takahashi K, Noguchi S, Takaku H, Koyanagi Y, Yamamoto N, Kawai G. J Biochem 138 583-592 (2005)
  9. Resolving fast and slow motions in the internal loop containing stem-loop 1 of HIV-1 that are modulated by Mg2+ binding: role in the kissing-duplex structural transition. Sun X, Zhang Q, Al-Hashimi HM. Nucleic Acids Res 35 1698-1713 (2007)
  10. Structure of the 30 kDa HIV-1 RNA Dimerization Signal by a Hybrid Cryo-EM, NMR, and Molecular Dynamics Approach. Zhang K, Keane SC, Su Z, Irobalieva RN, Chen M, Van V, Sciandra CA, Marchant J, Heng X, Schmid MF, Case DA, Ludtke SJ, Summers MF, Chiu W. Structure 26 490-498.e3 (2018)
  11. Structure of stem-loop IV of Tetrahymena telomerase RNA. Chen Y, Fender J, Legassie JD, Jarstfer MB, Bryan TM, Varani G. EMBO J 25 3156-3166 (2006)
  12. Rev regulates translation of human immunodeficiency virus type 1 RNAs. Groom HCT, Anderson EC, Dangerfield JA, Lever AML. J Gen Virol 90 1141-1147 (2009)
  13. MS3D structural elucidation of the HIV-1 packaging signal. Yu ET, Hawkins A, Eaton J, Fabris D. Proc Natl Acad Sci U S A 105 12248-12253 (2008)
  14. Rev binds specifically to a purine loop in the SL1 region of the HIV-1 leader RNA. Gallego J, Greatorex J, Zhang H, Yang B, Arunachalam S, Fang J, Seamons J, Lea S, Pomerantz RJ, Lever AM. J Biol Chem 278 40385-40391 (2003)
  15. Effects of a single amino acid substitution within the p2 region of human immunodeficiency virus type 1 on packaging of spliced viral RNA. Russell RS, Roldan A, Detorio M, Hu J, Wainberg MA, Liang C. J Virol 77 12986-12995 (2003)
  16. Three-dimensional RNA structure of the major HIV-1 packaging signal region. Stephenson JD, Li H, Kenyon JC, Symmons M, Klenerman D, Lever AM. Structure 21 951-962 (2013)
  17. Dissecting the protein-RNA and RNA-RNA interactions in the nucleocapsid-mediated dimerization and isomerization of HIV-1 stemloop 1. Hagan NA, Fabris D. J Mol Biol 365 396-410 (2007)
  18. Nucleocapsid protein-mediated maturation of dimer initiation complex of full-length SL1 stemloop of HIV-1: sequence effects and mechanism of RNA refolding. Mujeeb A, Ulyanov NB, Georgantis S, Smirnov I, Chung J, Parslow TG, James TL. Nucleic Acids Res 35 2026-2034 (2007)
  19. Understanding the isomerization of the HIV-1 dimerization initiation domain by the nucleocapsid protein. Turner KB, Hagan NA, Fabris D. J Mol Biol 369 812-828 (2007)
  20. Optimal packaging of FIV genomic RNA depends upon a conserved long-range interaction and a palindromic sequence within gag. Rizvi TA, Kenyon JC, Ali J, Aktar SJ, Phillip PS, Ghazawi A, Mustafa F, Lever AML. J Mol Biol 403 103-119 (2010)
  21. Sequences within both the 5' UTR and Gag are required for optimal in vivo packaging and propagation of mouse mammary tumor virus (MMTV) genomic RNA. Mustafa F, Al Amri D, Al Ali F, Al Sari N, Al Suwaidi S, Jayanth P, Philips PS, Rizvi TA. PLoS One 7 e47088 (2012)
  22. Consecutive GA pairs stabilize medium-size RNA internal loops. Chen G, Turner DH. Biochemistry 45 4025-4043 (2006)
  23. Zinc Fingers in HIV-1 Gag Precursor Are Not Equivalent for gRNA Recruitment at the Plasma Membrane. Boutant E, Bonzi J, Anton H, Nasim MB, Cathagne R, Réal E, Dujardin D, Carl P, Didier P, Paillart JC, Marquet R, Mély Y, de Rocquigny H, Bernacchi S. Biophys J 119 419-433 (2020)
  24. A genomic selection strategy to identify accessible and dimerization blocking targets in the 5'-UTR of HIV-1 RNA. Jakobsen MR, Damgaard CK, Andersen ES, Podhajska A, Kjems J. Nucleic Acids Res 32 e67 (2004)
  25. HIV RNA dimerisation interference by antisense oligonucleotides targeted to the 5' UTR structural elements. Reyes-Darias JA, Sánchez-Luque FJ, Berzal-Herranz A. Virus Res 169 63-71 (2012)
  26. Human immunodeficiency virus-1 Rev protein activates hepatitis C virus gene expression by directly targeting the HCV 5'-untranslated region. Qu J, Yang Z, Zhang Q, Liu W, Li Y, Ding Q, Liu F, Liu Y, Pan Z, He B, Zhu Y, Wu J. FEBS Lett 585 4002-4009 (2011)
  27. Molecular dynamics simulation for probing the flexibility of the 35 nucleotide SL1 sequence kissing complex from HIV-1Lai genomic RNA. Mazier S, Genest D. J Biomol Struct Dyn 24 471-479 (2007)
  28. An integrative NMR-SAXS approach for structural determination of large RNAs defines the substrate-free state of a trans-cleaving Neurospora Varkud Satellite ribozyme. Dagenais P, Desjardins G, Legault P. Nucleic Acids Res 49 11959-11973 (2021)
  29. HIV-1 Packaging Visualised by In-Gel SHAPE. D'Souza AR, Jayaraman D, Long Z, Zeng J, Prestwood LJ, Chan C, Kappei D, Lever AML, Kenyon JC. Viruses 13 2389 (2021)
  30. Insight into the intrinsic flexibility of the SL1 stem-loop from genomic RNA of HIV-1 as probed by molecular dynamics simulation. Mazier S, Genest D. Biopolymers 89 187-196 (2008)


Quick links