Structure and dynamics of the HIV-1 frameshift element RNA

Biochemistry

Volumn 53, Issue 26, 2014, Pages 4282-4291

  Low, Justin T ^a,b   Garcia Miranda, Pablo ^c   Mouzakis, Kathryn D ^c   Gorelick, Robert J ^d   Butcher, Samuel E ^c   Weeks, Kevin M ^a  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL MODIFICATION; OLIGONUCLEOTIDES; RNA;

CHEMICAL PROBING; COMPLEX STRUCTURE; DYNAMIC STRUCTURE; HELICAL CONFORMATION; PRIOR MODELING; STRUCTURAL ELEMENTS; STRUCTURE AND DYNAMICS; THERAPEUTIC TARGETS;

CONFORMATIONS;

FORMAMIDE; VIRUS RNA;

ARTICLE; BASE PAIRING; CONTROLLED STUDY; FRAMESHIFT MUTATION; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; NUCLEIC ACID STRUCTURE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RIBOSOMAL FRAMESHIFTING; RNA CONFORMATION; RNA FOLDING; SITE DIRECTED MUTAGENESIS; VIRION; VIRUS GENOME; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM;

FRAMESHIFTING, RIBOSOMAL; HIV-1; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RNA, VIRAL;

EID: 84903943879     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5004926     Document Type: Article

References (41)

1. Brierley, I., Ramos, and Dos, F. J. (2006) Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV Virus Res. 119, 29-42
2. Biswas, P., Jiang, X., Pacchia, A. L., Dougherty, J. P., and Peltz, S. W. (2004) The human immunodeficiency virus type 1 ribosomal frameshifting site is an invariant sequence determinant and an important target for antiviral therapy J. Virol. 78, 2082-2087
3. Shehu-Xhilaga, M., Crowe, S. M., and Mak, J. (2001) Maintenance of the Gag/Gag-Pol ratio is important for human immunodeficiency virus type 1 RNA dimerization and viral infectivity J. Virol. 75, 1834-1841
4. Brakier-Gingras, L., Charbonneau, J., and Butcher, S. E. (2012) Targeting frameshifting in the human immunodeficiency virus Expert Opin. Ther. Targets 16, 249-258
5. Gareiss, P. C. and Miller, B. L. (2009) Ribosomal frameshifting: an emerging drug target for HIV Curr. Opin Invest. Drugs 10, 121-128
6. Jacks, T., Power, M. D., Masiarz, F. R., Luciw, P. A., Barr, P. J., and Varmus, H. E. (1988) Characterization of ribosomal frameshifting in HIV-1 gag-pol expression Nature 331, 280-283
7. Le, S. Y., Shapiro, B. A., Chen, J. H., Nussinov, R., and Maizel, J. V. (1991) RNA pseudoknots downstream of the frameshift sites of retroviruses Genet. Anal. Technol. Appl. 8, 191-205
8. Du, Z., Giedroc, D. P., and 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
9. Huang, X., Yang, Y., Wang, G., Cheng, Q., and 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
10. Dinman, J. D., Richter, S., Plant, E. P., Taylor, R. C., Hammell, A. B., and Rana, T. M. (2002) The frameshift signal of HIV-1 involves a potential intramolecular triplex RNA structure Proc. Natl. Acad. Sci. U.S.A. 99, 5331-5336
11. Dulude, D., Baril, M., and Brakier-Gingras, L. (2002) Characterization of the frameshift stimulatory signal controlling a programmed -1 ribosomal frameshift in the human immunodeficiency virus type 1 Nucleic Acids Res. 30, 5094-5102
12. Gaudin, C., Mazauric, M.-H., Traïkia, M., Guittet, E., Yoshizawa, S., and Fourmy, D. (2005) Structure of the RNA signal essential for translational frameshifting in HIV-1 J. Mol. Biol. 349, 1024-1035
13. Staple, D. W. and Butcher, S. E. (2005) Solution structure and thermodynamic investigation of the HIV-1 frameshift inducing element J. Mol. Biol. 349, 1011-1023
14. Baril, M., Dulude, D., Gendron, K., Lemay, G., and Brakier-Gingras, L. (2003) Efficiency of a programmed -1 ribosomal frameshift in the different subtypes of the human immunodeficiency virus type 1 group M RNA 9, 1246-1253
15. Watts, J. M., Dang, K. K., Gorelick, R. J., Leonard, C. W., Bess, J. W., Swanstrom, R., Burch, C. L., and Weeks, K. M. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome Nature 460, 711-716
16. Merino, E. J., Wilkinson, K. A., Coughlan, J. L., and Weeks, K. M. (2005) RNA structure analysis at single nucleotide resolution by selective 2-hydroxyl acylation and primer extension (SHAPE) J. Am. Chem. Soc. 127, 4223-4231
17. Mathews, D. H., Disney, M. D., Childs, J. L., Schroeder, S. J., Zuker, M., and Turner, D. H. (2004) Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure Proc. Natl. Acad. Sci. U.S.A. 101, 7287-7292
18. Deigan, K. E., Li, T. W., Mathews, D. H., and Weeks, K. M. (2009) Accurate SHAPE-directed RNA structure determination Proc. Natl. Acad. Sci. U.S.A. 106, 97-102
19. Hajdin, C. E., Bellaousov, S., Huggins, W., Leonard, C. W., Mathews, D. H., and Weeks, K. M. (2013) Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots Proc. Natl. Acad. Sci. U.S.A. 110, 5498-5503
20. Jepsen, J. S., Sørensen, M. D., and Wengel, J. (2004) Locked nucleic acid: a potent nucleic acid analog in therapeutics and biotechnology Oligonucleotides 14, 130-146
21. Kaur, H., Babu, B. R., and Maiti, S. (2007) Perspectives on chemistry and therapeutic applications of Locked Nucleic Acid (LNA) Chem. Rev. 107, 4672-4697
22. Mouzakis, K. D., Lang, A. L., Vander Meulen, K. A., Easterday, P. D., and Butcher, S. E. (2013) HIV-1 frameshift efficiency is primarily determined by the stability of base pairs positioned at the mRNA entrance channel of the ribosome Nucleic Acids Res. 41, 1901-1913
23. Chertova, E., Bess, J. W., Crise, B. J., Sowder, R. C., II, Schaden, T. M., Hilburn, J. M., Hoxie, J. A., Benveniste, R. E., Lifson, J. D., Henderson, L. E., and Arthur, L. O. (2002) Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus J. Virol. 76, 5315-5325
24. Adachi, A., Koenig, S., Gendelman, H. E., Daugherty, D., Gattoni-Celli, S., Fauci, A. S., and Martin, M. A. (1987) Productive, persistent infection of human colorectal cell lines with human immunodeficiency virus J. Virol. 61, 209-213
25. Means, R. E., Matthews, T., Hoxie, J. A., Malim, M. H., Kodama, T., and Desrosiers, R. C. (2001) Ability of the V3 loop of simian immunodeficiency virus to serve as a target for antibody-mediated neutralization: correlation of neutralization sensitivity, growth in macrophages, and decreased dependence on CD4 J. Virol. 75, 3903-3915
26. Gherghe, C., Lombo, T., Leonard, C. W., Datta, S. A. K., Bess, J. W., Gorelick, R. J., Rein, A., and Weeks, K. M. (2010) Definition of a high-affinity Gag recognition structure mediating packaging of a retroviral RNA genome Proc. Natl. Acad. Sci. U.S.A. 107, 19248-19253
27. Ott, D. E., Coren, L. V., Johnson, D. G., Sowder, R. C., Arthur, L. O., and Henderson, L. E. (1995) Analysis and localization of cyclophilin A found in the virions of human immunodeficiency virus type 1 MN strain AIDS Res. Hum. Retroviruses 11, 1003-1006
28. Karabiber, F., McGinnis, J. L., Favorov, O. V., and Weeks, K. M. (2013) QuShape: rapid, accurate, and best-practices quantification of nucleic acid probing information, resolved by capillary electrophoresis RNA 19, 63-73
29. McGinnis, J. L., Duncan, C. D. S., and Weeks, K. M. (2009) High-throughput SHAPE and hydroxyl radical analysis of RNA structure and ribonucleoprotein assembly Methods Enzymol. 468, 67-89
30. Mortimer, S. A. and Weeks, K. M. (2007) A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry J. Am. Chem. Soc. 129, 4144-4145
31. Steen, K.-A., Rice, G. M., and Weeks, K. M. (2012) Fingerprinting noncanonical and tertiary RNA structures by differential SHAPE reactivity J. Am. Chem. Soc. 134, 13160-13163
32. Rice, G. M., Leonard, C. W., and Weeks, K. M. (2014) RNA secondary structure modeling at consistent high accuracy using differential SHAPE RNA 20, 846-854
33. Blake, R. D. and Delcourt, S. G. (1996) Thermodynamic effects of formamide on DNA stability Nucleic Acids Res. 24, 2095-2103
34. Marcheschi, R. J., Tonelli, M., Kumar, A., and Butcher, S. E. (2011) Structure of the HIV-1 frameshift site RNA bound to a small molecule inhibitor of viral replication ACS Chem. Biol. 6, 857-864
35. 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, e96
36. Tyrrell, J., McGinnis, J. L., Weeks, K. M., and Pielak, G. J. (2013) The cellular environment stabilizes adenine riboswitch RNA structure Biochemistry 52, 8777-8785
37. Gendron, K., Charbonneau, J., Dulude, D., Heveker, N., Ferbeyre, G., and Brakier-Gingras, L. (2008) The presence of the TAR RNA structure alters the programmed -1 ribosomal frameshift efficiency of the human immunodeficiency virus type 1 (HIV-1) by modifying the rate of translation initiation Nucleic Acids Res. 36, 30-40
38. Doyon, L., Croteau, G., Thibeault, D., Poulin, F., Pilote, L., and Lamarre, D. (1996) Second locus involved in human immunodeficiency virus type 1 resistance to protease inhibitors J. Virol. 70, 3763-3769
39. Doyon, L., Payant, C., Brakier-Gingras, L., and Lamarre, D. (1998) Novel Gag-Pol frameshift site in human immunodeficiency virus type 1 variants resistant to protease inhibitors J. Virol. 72, 6146-6150
40. Girnary, R., King, L., Robinson, L., Elston, R., and Brierley, I. (2007) Structure-function analysis of the ribosomal frameshifting signal of two human immunodeficiency virus type 1 isolates with increased resistance to viral protease inhibitors J. Gen. Virol. 88, 226-235
41. Houck-Loomis, B., Durney, M. A., Salguero, C., Shankar, N., Nagle, J. M., Goff, S. P., and D'Souza, V. M. (2011) An equilibrium-dependent retroviral mRNA switch regulates translational recoding Nature 480, 561-564