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Research Articles

A potential long-range RNA-RNA interaction in the HIV-1 RNA

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Pages 14968-14976 | Received 03 Jul 2022, Accepted 19 Feb 2023, Published online: 02 Mar 2023

References

  • Abbink, T. E., & Berkhout, B. (2003). A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the Gag start codon. The Journal of Biological Chemistry, 278(13), 11601–11611. https://doi.org/10.1074/jbc.M210291200
  • Andersen, E. S., Contera, S. A., Knudsen, B., Damgaard, C. K., Besenbacher, F., & Kjems, J. (2004). Role of the trans-activation response element in dimerization of HIV-1 RNA. The Journal of Biological Chemistry, 279(21), 22243–22249. https://doi.org/10.1074/jbc.M314326200
  • Barry, J. K., & Miller, W. A. (2002). A-1 ribosomal frameshift element that requires base pairing across four kilobases suggests a mechanism of regulating ribosome and replicase traffic on a viral RNA. Proceedings of the National Academy of Sciences of the United States of America, 99(17), 11133–11138. https://doi.org/10.1073/pnas.162223099
  • Beerens, N., & Kjems, J. (2010). Circularization of the HIV-1 genome facilitates strand transfer during reverse transcription. RNA, 16(6), 1226–1235. https://doi.org/10.1261/rna.2039610
  • Braun, F., Durand, S., & Condon, C. (2017). Initiating ribosomes and a 5'/3'-UTR interaction control ribonuclease action to tightly couple B. subtilis hbs mRNA stability with translation. Nucleic Acids Research, 45, 11386–11400.
  • Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., GrosseKunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., & Warren, G. L. (1998). Crystallography + NMR system: A new software suite for macromolecular structure determination. Acta Crystallographica. Section D, Biological Crystallography, D54, 905–921.
  • Chen, J., & Kastan, M. B. (2010). 5'-3'-UTR interactions regulate p53 mRNA translation and provide a target for modulating p53 induction after DNA damage. Genes & Development, 24(19), 2146–2156. https://doi.org/10.1101/gad.1968910
  • Chkuaseli, T., & White, K. A. (2018). Intragenomic long-distance RNA-RNA interactions in plus-strand RNA plant viruses. Frontiers in Microbiology, 9, 529. https://doi.org/10.3389/fmicb.2018.00529
  • Choi, I. R., Ostrovsky, M., Zhang, G., & White, K. A. (2001). Regulatory activity of distal and core RNA elements in Tombusvirus subgenomic mRNA2 transcription. The Journal of Biological Chemistry, 276(45), 41761–41768. https://doi.org/10.1074/jbc.M106727200
  • Choi, I. R., & White, K. A. (2002). An RNA activator of subgenomic mRNA1 transcription in tomato bushy stunt virus. The Journal of Biological Chemistry, 277(5), 3760–3766. https://doi.org/10.1074/jbc.M109067200
  • Cimino, P. A., Nicholson, B. L., Wu, B., Xu, W., & White, K. A. (2011). Multifaceted regulation of translational readthrough by RNA replication elements in a tombusvirus. PLoS Pathogens, 7, e1002423.
  • Dam, E., Pleij, K., & Draper, D. (1992). Structural and functional aspects of RNA pseudoknots. Biochemistry, 31, 11665–11676.
  • Du, Z., Giedroc, D. P., & Hoffman, D. W. (1996). Structure of the autoregulatory pseudoknot within the gene 32 messenger RNA of bacteriophages T2 and T6: A model for a possible family of structurally related RNA pseudoknots. Biochemistry, 35, 4187–4198.
  • Du, Z., & Hoffman, D. W. (1997). An NMR and mutational study of the pseudoknot within the gene 32 mRNA of bacteriophage T2: Insights into a family of structurally related RNA pseudoknots. Nucleic Acids Research, 25(6), 1130–1135. https://doi.org/10.1093/nar/25.6.1130
  • Fabian, M. R., & White, K. A. (2004). 5'-3' RNA-RNA interaction facilitates cap- and poly(A) tail-independent translation of tomato bushy stunt virus mrna: A potential common mechanism for tombusviridae. The Journal of Biological Chemistry, 279(28), 28862–28872. https://doi.org/10.1074/jbc.M401272200
  • Fabian, M. R., & White, K. A. (2006). Analysis of a 3'-translation enhancer in a tombusvirus: A dynamic model for RNA-RNA interactions of mRNA termini. RNA, 12, 1304–1314.
  • Guo, L., Allen, E. M., & Miller, W. A. (2001). Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Molecular Cell, 7(5), 1103–1109. https://doi.org/10.1016/s1097-2765(01)00252-0
  • Hu, B., Pillai-Nair, N., & Hemenway, C. (2007). Long-distance RNA-RNA interactions between terminal elements and the same subset of internal elements on the potato virus X genome mediate minus- and plus-strand RNA synthesis. RNA, 13(2), 267–280. https://doi.org/10.1261/rna.243607
  • Huang, S. W., Chan, M. Y., Hsu, W. L., Huang, C. C., & Tsai, C. H. (2012). The 3'-terminal hexamer sequence of classical swine fever virus RNA plays a role in negatively regulating the IRES-mediated translation. PLoS One, 7, e33764.
  • Huang, X., Cheng, Q., & Du, Z. (2013a). A genome-wide analysis of RNA pseudoknots that stimulate efficient-1 ribosomal frameshifting or readthrough in animal viruses. BioMed Research International, 2013, 984028. https://doi.org/10.1155/2013/984028
  • Huang, X., Cheng, Q., & Du, Z. (2013b). Possible utilization of -1 Ribosomal frame shifting in the expression of a human SEMA6C isoform. Bioinformation, 9, 736–738.
  • Huang, X., Du, Z., Cheng, J., & Cheng, Q. (2013). PKscan: A program to identify H-type RNA pseudoknots in any RNA sequence with unlimited length. Bioinformation, 9, 440–442.
  • Huang, X., Yang, Y., Wang, G., Cheng, Q., & Du, Z. (2014). Highly conserved RNA pseudoknots at the gag-pol junction of HIV-1 suggest a novel mechanism of -1 ribosomal frameshifting. RNA, 20, 587–593.
  • Huthoff, H., & Berkhout, B. (2001). Mutations in the TAR hairpin affect the equilibrium between alternative conformations of the HIV-1 leader RNA. Nucleic Acids Research, 29(12), 2594–2600. https://doi.org/10.1093/nar/29.12.2594
  • Ishimaru, D., Plant, E. P., Sims, A. C., Yount, B. L., Jr., Roth, B. M., Eldho, N. V., Pérez-Alvarado, G. C., Armbruster, D. W., Baric, R. S., Dinman, J. D., Taylor, D. R., & Hennig, M. (2013). RNA dimerization plays a role in ribosomal frameshifting of the SARS coronavirus. Nucleic Acids Research, 41, 2594–2608.
  • Kalloush, R. M., Vivet-Boudou, V., Ali, L. M., Mustafa, F., Marquet, R., & Rizvi, T. A. (2016). Packaging of Mason-Pfizer monkey virus (MPMV) genomic RNA depends upon conserved long-range interactions (LRIs) between U5 and gag sequences. RNA, 22(6), 905–919. https://doi.org/10.1261/rna.055731.115
  • Kim, K. H., & Hemenway, C. L. (1999). Long-distance RNA-RNA interactions and conserved sequence elements affect potato virus X plus-strand RNA accumulation. RNA, 5(5), 636–645. https://doi.org/10.1017/s1355838299982006
  • Klovins, J., Berzins, V., & van Duin, J. (1998). A long-range interaction in Qbeta RNA that bridges the thousand nucleotides between the M-site and the 3' end is required for replication. RNA, 4(8), 948–957. https://doi.org/10.1017/s1355838298980177
  • Licis, N., van Duin, J., Balklava, Z., & Berzins, V. (1998). Long-range translational coupling in single-stranded RNA bacteriophages: An evolutionary analysis. Nucleic Acids Research, 26(13), 3242–3246. https://doi.org/10.1093/nar/26.13.3242
  • Lin, H. X., & White, K. A. (2004). A complex network of RNA-RNA interactions controls subgenomic mRNA transcription in a tombusvirus. EMBO Journal, 23, 3365–3374.
  • Liu, Y., Wimmer, E., & Paul, A. V. (2009). Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochimica et Biophysica Acta, 1789(9-10), 495–517. https://doi.org/10.1016/j.bbagrm.2009.09.007
  • López de Quinto, S., Sáiz, M., de la Morena, D., Sobrino, F., & Martínez-Salas, E. (2002). IRES-driven translation is stimulated separately by the FMDV 3'-NCR and poly(A) sequences. Nucleic Acids Research, 30(20), 4398–4405. https://doi.org/10.1093/nar/gkf569
  • Lovci, M. T., Ghanem, D., Marr, H., Arnold, J., Gee, S., Parra, M., Liang, T. Y., Stark, T. J., Gehman, L. T., Hoon, S., Massirer, K. B., Pratt, G. A., Black, D. L., Gray, J. W., Conboy, J. G., & Yeo, G. W. (2013). Rbfox proteins regulate alternative mRNA splicing through evolutionarily conserved RNA bridges. Nature Structural & Molecular Biology, 20, 1434–1442.
  • Mateos-Gomez, P. A., Morales, L., Zuñiga, S., Enjuanes, L., & Sola, I. (2013). Long-distance RNA-RNA interactions in the coronavirus genome form high-order structures promoting discontinuous RNA synthesis during transcription. Journal of Virology, 87(1), 177–186. https://doi.org/10.1128/JVI.01782-12
  • Miller, W. A., & White, K. A. (2006). Long-distance RNA-RNA interactions in plant virus gene expression and replication. Annual Review of Phytopathology, 44, 447–467. https://doi.org/10.1146/annurev.phyto.44.070505.143353
  • Nicholson, B. L., & White, K. A. (2008). Context-influenced cap-independent translation of Tombusvirus mRNAs in vitro. Virology, 380(2), 203–212. https://doi.org/10.1016/j.virol.2008.08.003
  • Nicholson, B. L., & White, K. A. (2011). 3' Cap-independent translation enhancers of positive-strand RNA plant viruses. Current Opinion in Virology, 1(5), 373–380. https://doi.org/10.1016/j.coviro.2011.10.002
  • Nicholson, B. L., & White, K. A. (2014). Functional long-range RNA-RNA interactions in positive-strand RNA viruses. Nature Reviews. Microbiology, 12(7), 493–504. https://doi.org/10.1038/nrmicro3288
  • Nicholson, B. L., Zaslaver, O., Mayberry, L. K., Browning, K. S., & White, K. A. (2013). Tombusvirus Y-shaped translational enhancer forms a complex with eIF4F and can be functionally replaced by heterologous translational enhancers. Journal of Virology, 87(3), 1872–1883. https://doi.org/10.1128/JVI.02711-12
  • Ooms, M., Abbink, T. E., Pham, C., & Berkhout, B. (2007). Circularization of the HIV-1 RNA genome. Nucleic Acids Research, 35(15), 5253–5261. https://doi.org/10.1093/nar/gkm564
  • Paillart, J. C., Skripkin, E., Ehresmann, B., Ehresmann, C., & Marquet, R. (2002). In vitro evidence for a long range pseudoknot in the 5'-untranslated and matrix coding regions of HIV-1 genomic RNA. The Journal of Biological Chemistry, 277(8), 5995–6004. https://doi.org/10.1074/jbc.M108972200
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera—A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
  • Pleij, C. W. (1990). Pseudoknots: A new motif in the RNA game. Trends in Biochemical Science, 15, 143–147.
  • Pleij, C. W., Rietveld, K., & Bosch, L. (1985). A new principle of RNA folding based on pseudoknotting. Nucleic Acids Research, 13(5), 1717–1731. https://doi.org/10.1093/nar/13.5.1717
  • Pollom, E., Dang, K. K., Potter, E. L., Gorelick, R. J., Burch, C. L., Weeks, K. M., & Swanstrom, R. (2013). Comparison of SIV and HIV-1 genomic RNA structures reveals impact of sequence evolution on conserved and non-conserved structural motifs. PLoS Pathogens, 9(4), e1003294. https://doi.org/10.1371/journal.ppat.1003294
  • Rakotondrafara, A. M., Polacek, C., Harris, E., & Miller, W. A. (2006). Oscillating kissing stem-loop interactions mediate 5' scanning-dependent translation by a viral 3'-cap-independent translation element. RNA, 12(10), 1893–1906. https://doi.org/10.1261/rna.115606
  • Romero-López, C., Barroso-Deljesus, A., García-Sacristán, A., Briones, C., & Berzal-Herranz, A. (2012). The folding of the hepatitis C virus internal ribosome entry site depends on the 3'-end of the viral genome. Nucleic Acids Research, 40, 11697–11713.
  • Romero-López, C., & Berzal-Herranz, A. (2009). A long-range RNA-RNA interaction between the 5' and 3' ends of the HCV genome. RNA, 15(9), 1740–1752. https://doi.org/10.1261/rna.1680809
  • Romero-López, C., & Berzal-Herranz, A. (2012). The functional RNA domain 5BSL3.2 within the NS5B coding sequence influences hepatitis C virus IRES-mediated translation. Cellular and Molecular Life Sciences, 69(1), 103–113. https://doi.org/10.1007/s00018-011-0729-z
  • Ruiz de los Mozos, I., Vergara-Irigaray, M., Segura, V., Villanueva, M., Bitarte, N., Saramago, M., Domingues, S., Arraiano, C. M., Fechter, P., Romby, P., Valle, J., Solano, C., Lasa, I., & Toledo-Arana, A. (2013). Base pairing interaction between 5'- and 3'-UTRs controls icaR mRNA translation in Staphylococcus aureus. PLoS Genetics, 9, e1004001.
  • Serrano, P., Pulido, M. R., Sáiz, M., & Martínez-Salas, E. (2006). The 3' end of the foot-and-mouth disease virus genome establishes two distinct long-range RNA-RNA interactions with the 5' end region. The Journal of General Virology, 87(Pt 10), 3013–3022. https://doi.org/10.1099/vir.0.82059-0
  • Simon, A. E., & Miller, W. A. (2013). 3' cap-independent translation enhancers of plant viruses. Annual Review of Microbiology, 67, 21–42. https://doi.org/10.1146/annurev-micro-092412-155609
  • Skittrall, J. P., Ingemarsdotter, C. K., Gog, J. R., & Lever, A. M. L. (2019). A scale-free analysis of the HIV-1 genome demonstrates multiple conserved regions of structural and functional importance. PLoS Computational Biology, 15(9), e1007345. https://doi.org/10.1371/journal.pcbi.1007345
  • Sükösd, Z., Andersen, E. S., Seemann, S. E., Jensen, M. K., Hansen, M., Gorodkin, J., & Kjems, J. (2015). Full-length RNA structure prediction of the HIV-1 genome reveals a conserved core domain. Nucleic Acids Research, 43(21), 10168–10179. https://doi.org/10.1093/nar/gkv1039
  • Tajima, Y., Iwakawa, H. O., Kaido, M., Mise, K., & Okuno, T. (2011). A long-distance RNA-RNA interaction plays an important role in programmed -1 ribosomal frameshifting in the translation of p88 replicase protein of Red clover necrotic mosaic virus. Virology, 417(1), 169–178. https://doi.org/10.1016/j.virol.2011.05.012
  • Treder, K., Kneller, E. L., Allen, E. M., Wang, Z., Browning, K. S., & Miller, W. A. (2008). The 3' cap-independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA, 14(1), 134–147. https://doi.org/10.1261/rna.777308
  • van Himbergen, J., van Geffen, B., & van Duin, J. (1993). Translational control by a long range RNA-RNA interaction; a basepair substitution analysis. Nucleic Acids Research, 21(8), 1713–1717. https://doi.org/10.1093/nar/21.8.1713
  • Wang, S., Mortazavi, L., & White, K. A. (2008). Higher-order RNA structural requirements and small-molecule induction of tombusvirus subgenomic mRNA transcription. Journal of Virology, 82(8), 3864–3871. https://doi.org/10.1128/JVI.02416-07
  • Watts, J. M., Dang, K. K., Gorelick, R. J., Leonard, C. W., Bess, J. W., Jr., Swanstrom, R., Burch, C. L., & Weeks, K. M. (2009). Architecture and secondary structure of an entire HIV-1 RNA genome. Nature, 460(7256), 711–716. https://doi.org/10.1038/nature08237
  • Wu, B., Pogany, J., Na, H., Nicholson, B. L., Nagy, P. D., & White, K. A. (2009). A discontinuous RNA platform mediates RNA virus replication: Building an integrated model for RNA-based regulation of viral processes. PLoS Pathogens, 5(3), e1000323. https://doi.org/10.1371/journal.ppat.1000323

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