A novel combined RNA-protein interaction analysis distinguishes HIV-1 Gag protein binding sites from structural change in the viral RNA leader

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Kenyon, Julia C ^a   Prestwood, Liam J ^a   Lever, Andrew M L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

5' UNTRANSLATED REGION; GAG PROTEIN; PROTEIN BINDING; TRANSACTIVATOR PROTEIN; VIRUS RNA;

5' UNTRANSLATED REGION; BINDING SITE; CHEMISTRY; CONFORMATION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; LONG TERMINAL REPEAT; METABOLISM; MOLECULAR BIOLOGY; MOLECULAR GENETICS; MOLECULAR MODEL; MUTATION; NUCLEOTIDE SEQUENCE; PROCEDURES; PROTEIN TERTIARY STRUCTURE; REPRODUCIBILITY; VIRUS GENOME;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; BINDING SITES; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENOME, VIRAL; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; MODELS, MOLECULAR; MOLECULAR BIOLOGY; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REPRODUCIBILITY OF RESULTS; RNA, VIRAL; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84943742970     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14369     Document Type: Article

References (43)

1. Stephenson, J. D. et al. Three-dimensional RNA structure of the major HIV-1 packaging signal region. Structure 21, 951-62 (2013).
2. Peselis, A. & Serganov, A. Themes and variations in riboswitch structure and function. Biochim Biophys Acta 1839(10), 908-918 (2014).
3. Wohrl, B. M., Ehresmann, B., Keith, G. & Le Grice, S. F. Nuclease footprinting of human immunodeficiency virus reverse transcriptase/tRNA(Lys-3) complexes. J Biol Chem 268, 13617-24 (1993).
4. Costa, M. & Monachello, D. Probing RNA folding by hydroxyl radical footprinting. Methods Mol Biol 1086, 119-42 (2014).
5. Kenyon, J., Prestwood, L. & Lever, A. Current perspectives on RNA secondary structure probing. Biochem Soc Trans 42, 1251-5 (2014).
6. WHO. Global report: UNAIDS report on the global AIDS epidemic 2013. in WHO Library Cataloguing-in-Publication Data Vol. UNAIDS/JC2502/1/E (2013).
7. Kuzembayeva, M., Dilley, K., Sardo, L. & Hu, W. S. Life of psi: how full-length HIV-1 RNAs become packaged genomes in the viral particles. Virology 454-455, 362-70 (2014).
8. Nikolaitchik, O. A. et al. Dimeric RNA recognition regulates HIV-1 genome packaging. PLoS Pathog 9, e1003249 (2013).
9. Lever, A. M. HIV-1 R. N. A. packaging. Adv Pharmacol 55, 1-32 (2007).
10. D'Souza, V. & Summers, M. F. How retroviruses select their genomes. Nat Rev Microbiol 3, 643-55 (2005).
11. Jouvenet, N., Bieniasz, P. D. & Simon, S. M. Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454, 236-40 (2008).
12. Lu, K. et al. NMR detection of structures in the HIV-1 5' -leader RNA that regulate genome packaging. Science 334, 242-5 (2011).
13. Kenyon, J. C., Prestwood, L. J., Le Grice, S. F. & Lever, A. M. In-gel probing of individual RNA conformers within a mixed population reveals a dimerization structural switch in the HIV-1 leader. Nucleic Acids Res 41, e174 (2013).
14. Damgaard, C. K., 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 26, 3667-76 (1998).
15. Wilkinson, K. A. et al. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol 6, e96 (2008).
16. Kuhn-Holsken, E., Dybkov, O., Sander, B., Luhrmann, R. & Urlaub, H. Improved identification of enriched peptide RNA crosslinks from ribonucleoprotein particles (RNPs) by mass spectrometry. Nucleic Acids Res 35, e95 (2007).
17. Shetlar, M. D., Carbone, J., Steady, E. & Hom, K. Photochemical addition of amino acids and peptides to polyuridylic acid. Photochem Photobiol 39, 141-4 (1984).
18. Shetlar, M. D. et al. Photochemical addition of amino acids and peptides to homopolyribonucleotides of the major DNA bases. Photochem Photobiol 39, 135-40 (1984).
19. Kramer, K. et al. Photo-cross-linking and high-resolution mass spectrometry for assignment of RNA-binding sites in RNAbinding proteins. Nat Methods doi: 10.1016/j.ymeth.2015.06.005. (2014).
20. Konig, J. et al. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol 17, 909-15 (2010).
21. Urlaub, H., Hartmuth, K., Kostka, S., Grelle, G. & Luhrmann, R. A general approach for identification of RNA-protein crosslinking sites within native human spliceosomal small nuclear ribonucleoproteins (snRNPs). Analysis of RNA-protein contacts in native U1 and U4/U6.U5 snRNPs. J Biol Chem 275, 41458-68 (2000).
22. Calnan, B. J., Biancalana, S., Hudson, D. & Frankel, A. D. Analysis of arginine-rich peptides from the HIV Tat protein reveals unusual features of RNA-protein recognition. Genes Dev 5, 201-10 (1991).
23. Cordingley, M. G. et al. Sequence-specific interaction of Tat protein and Tat peptides with the transactivation-responsive sequence element of human immunodeficiency virus type 1 in vitro. Proc Natl Acad Sci USA 87, 8985-9 (1990).
24. Weeks, K. M., Ampe, C., Schultz, S. C., Steitz, T. A. & Crothers, D. M. Fragments of the HIV-1 Tat protein specifically bind TAR RNA. Science 249, 1281-5 (1990).
25. Frankel, A. D. Peptide models of the Tat-TAR protein-RNA interaction. Protein Sci 1, 1539-42 (1992).
26. Zacharias, M. & Hagerman, P. J. The bend in RNA created by the trans-activation response element bulge of human immunodeficiency virus is straightened by arginine and by Tat-derived peptide. Proc Natl Acad Sci USA 92, 6052-6 (1995).
27. Merino, E. J., Wilkinson, K. A., Coughlan, J. L. & Weeks, K. M. RNA structure analysis at single nucleotide resolution by selective 2' -hydroxyl acylation and primer extension (SHAPE). J Am Chem Soc 127, 4223-31 (2005).
28. Aboul-ela, F., Karn, J. & Varani, G. The structure of the human immunodeficiency virus type-1 TAR RNA reveals principles of RNA recognition by Tat protein. J Mol Biol 253, 313-32 (1995).
29. 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 12, 40 (2015).
30. Horn, W. T. et al. The crystal structure of a high affinity RNA stem-loop complexed with the bacteriophage MS2 capsid: further challenges in the modeling of ligand-RNA interactions. RNA 10, 1776-82 (2004).
31. Moore, M. D. & Hu, W. S. HIV-1 RNA dimerization: It takes two to tango. AIDS Rev 11, 91-102 (2009).
32. Campbell, S. & Rein, A. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J Virol 73, 2270-9 (1999).
33. Kramer, K. et al. Photo-cross-linking and high-resolution mass spectrometry for assignment of RNA-binding sites in RNAbinding proteins. Nat Methods 11, 1064-70 (2014).
34. Bell, N. M., Kenyon, J. C., Balasubramanian, S. & Lever, A. M. Comparative structural effects of HIV-1 Gag and nucleocapsid proteins in binding to and unwinding of the viral RNA packaging signal. Biochemistry 51, 3162-9 (2012).
35. Abd El-Wahab, E. W. et al. Specific recognition of the HIV-1 genomic RNA by the Gag precursor. Nat Commun 5, 4304 (2014).
36. Lu, K., Heng, X. & Summers, M. F. Structural determinants and mechanism of HIV-1 genome packaging. J Mol Biol 410, 609-33 (2011).
37. Urlaub, H., Raker, V. A., Kostka, S. & Luhrmann, R. Sm protein-Sm site RNA interactions within the inner ring of the spliceosomal snRNP core structure. EMBO J 20, 187-96 (2001).
38. De Guzman, R. N. et al. Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science 279, 384-8 (1998).
39. Paillart, J. C., Skripkin, E., Ehresmann, B., Ehresmann, C. & Marquet, R. In vitro evidence for a long range pseudoknot in the 5' -untranslated and matrix coding regions of HIV-1 genomic RNA. J Biol Chem 277, 5995-6004 (2002).
40. Russell, R. S., Liang, C. & Wainberg, M. A. Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably? Retrovirology 1, 23 (2004).
41. Kutluay, S. B. et al. Global Changes in the RNA Binding Specificity of HIV-1 Gag Regulate Virion Genesis. Cell 159, 1096-109 (2014).
42. Fisher, A. G., Collalti, E., Ratner, L., Gallo, R. C. & Wong-Staal, F. A molecular clone of HTLV-III with biological activity. Nature 316, 262-5 (1985).
43. Vasa, S. M., Guex, N., Wilkinson, K. A., Weeks, K. M. & Giddings, M. C. ShapeFinder: a software system for high-throughput quantitative analysis of nucleic acid reactivity information resolved by capillary electrophoresis. RNA 14, 1979-90 (2008).