The in vitro loose dimer structure and rearrangements of the HIV-2 leader RNA

Nucleic Acids Research

Volumn 39, Issue 16, 2011, Pages 7234-7248

  Purzycka, Katarzyna J ^a   Pachulska Wieczorek, Katarzyna ^a   Adamiak, Ryszard W ^a  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DIMER; NCP8 PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; GENE REARRANGEMENT; HUMAN IMMUNODEFICIENCY VIRUS 2; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE BINDING SITE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA FINGERPRINTING; RNA HYBRIDIZATION; RNA PROBE; RNA STRUCTURE; STRUCTURE ANALYSIS; VIRUS RECOMBINANT;

5' UNTRANSLATED REGIONS; BINDING SITES; CAPSID PROTEINS; DIMERIZATION; HIV-2; NUCLEIC ACID CONFORMATION; RNA, VIRAL; RNA-BINDING PROTEINS;

HUMAN IMMUNODEFICIENCY VIRUS 2;

EID: 80052506027     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr385     Document Type: Article

References (54)

1. Kaye, J.F. and Lever, A.M. (1998) Nonreciprocal packaging of human immunodeficiency virus type 1 and type 2 RNA: a possible role for the p2 domain of Gag in RNA encapsidation. J. Virol., 72, 5877-5885. (Pubitemid 28283375)
2. Rabson, A.B. and Graves, B.J. (1997) Synthesis and processing of viral RNA. In Coffin, J.M., Hughes, S.H. and Vink, M. (eds), Retroviruses. Cold Spring Harbor Laboratory Press, New York, pp. 205-262.
3. Skripkin, E., Paillart, J.C., Marquet, R., Ehresmann, B. and Ehresmann, C. (1994) Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proc. Natl Acad. Sci. USA, 91, 4945-4949. (Pubitemid 24177767)
4. McBride, M.S. and Panganiban, A.T. (1996) The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J. Virol., 70, 2963-2973. (Pubitemid 26121910)
5. Paillart, J.C., Marquet, R., Skripkin, E., Ehresmann, C. and Ehresmann, B. (1996) Dimerization of retroviral genomic RNAs: structural and functional implications. Biochimie, 78, 639-653. (Pubitemid 26397590)
6. Berkhout, B. and van Wamel, J.L. (1996) Role of the DIS hairpin in replication of human immunodeficiency virus type 1. J. Virol., 70, 6723-6732. (Pubitemid 26307379)
7. 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.
8. Baig, T.T., Strong, C.L., Lodmell, J.S. and Lanchy, J.M. (2008) Regulation of primate lentiviral RNA dimerization by structural entrapment. Retrovirology, 5, 65.
9. Lanchy, J.M., Rentz, C.A., Ivanovitch, J.D. and Lodmell, J.S. (2003) Elements located upstream and downstream of the major splice donor site influence the ability of HIV-2 leader RNA to dimerize in vitro. Biochemistry, 42, 2634-2642. (Pubitemid 36330617)
10. Jossinet, F., Lodmell, J.S., Ehresmann, C., Ehresmann, B. and Marquet, R. (2001) Identification of the in vitro HIV-2/SIV RNA dimerization site reveals striking differences with HIV-1. J. Biol. Chem., 276, 5598-5604.
11. Dirac, A.M., Huthoff, H., Kjems, J. and Berkhout, B. (2001) The dimer initiation site hairpin mediates dimerization of the human immunodeficiency virus, type 2 RNA genome. J. Biol. Chem., 276, 32345-32352.
12. Lanchy, J.M., Ivanovitch, J.D. and Lodmell, J.S. (2003) A structural linkage between the dimerization and encapsidation signals in HIV-2 leader RNA. RNA, 9, 1007-1018. (Pubitemid 36899243)
13. Lanchy, J.M. and Lodmell, J.S. (2002) Alternate usage of two dimerization initiation sites in HIV-2 viral RNA in vitro. J. Mol. Biol., 319, 637-648.
14. Berkhout, B., Essink, B.B. and Schoneveld, I. (1993) In vitro dimerization of HIV-2 leader RNA in the absence of PuGGAPuA motifs. FASEB J., 7, 181-187. (Pubitemid 23034032)
15. Andersen, E.S., Contera, S.A., Knudsen, B., Damgaard, C.K., Besenbacher, F. and Kjems, J. (2004) Role of the trans-activation response element in dimerization of HIV-1 RNA. J. Biol. Chem., 279, 22243-22249. (Pubitemid 38679420)
16. Huthoff, H. and Berkhout, B. (2001) Two alternating structures of the HIV-1 leader RNA. RNA., 7, 143-157. (Pubitemid 32381937)
17. Dirac, A.M., Huthoff, H., Kjems, J. and Berkhout, B. (2002) Regulated HIV-2 RNA dimerization by means of alternative RNA conformations. Nucleic Acids Res., 30, 2647-2655. (Pubitemid 34679770)
18. Paillart, J.C., Dettenhofer, M., Yu, X.F., Ehresmann, C., Ehresmann, B. and Marquet, R. (2004) First snapshots of the HIV-1 RNA structure in infected cells and in virions. J. Biol. Chem., 279, 48397-48403. (Pubitemid 39540996)
19. Griffin, S.D., Allen, J.F. and Lever, A.M. (2001) The major human immunodeficiency virus type 2 (HIV-2) packaging signal is present on all HIV-2 RNA species: cotranslational RNA encapsidation and limitation of Gag protein confer specificity. J. Virol., 75, 12058-12069. (Pubitemid 33115878)
20. L'Hernault, A., Greatorex, J.S., Crowther, R.A. and Lever, A.M. (2007) Dimerisation of HIV-2 genomic RNA is linked to efficient RNA packaging, normal particle maturation and viral infectivity. Retrovirology, 4, 90.
21. Lanchy, J.M. and Lodmell, J.S. (2007) An extended stem-loop 1 is necessary for human immunodeficiency virus type 2 replication and affects genomic RNA encapsidation. J. Virol., 81, 3285-3292. (Pubitemid 46456637)
22. Lanchy, J.M., Szafran, Q.N. and Lodmell, J.S. (2004) Splicing affects presentation of RNA dimerization signals in HIV-2 in vitro. Nucleic Acids Res., 32, 4585-4595. (Pubitemid 39317736)
23. Berkhout, B. (1996) Structure and function of the human immunodeficiency virus leader RNA. Prog. Nucleic Acid Res. Mol. Biol., 54, 1-34.
24. Baig, T.T., Lanchy, J.M. and Lodmell, J.S. (2007) HIV-2 RNA dimerization is regulated by intramolecular interactions in vitro. RNA, 13, 1341-1354. (Pubitemid 47080478)
25. Abbink, T.E. and Berkhout, B. (2003) A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the Gag start codon. J. Biol. Chem., 278, 11601-11611. (Pubitemid 36792722)
26. Rein, A., Henderson, L.E. and Levin, J.G. (1998) Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem. Sci., 23, 297-301. (Pubitemid 28461895)
27. Damgaard, C.K., Dyhr-Mikkelsen, H. and Kjems, J. (1998) 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, 3667-3676. (Pubitemid 28367971)
28. De Guzman, R.N., Wu, Z.R., Stalling, C.C., Pappalardo, L., Borer, P.N. and Summers, M.F. (1998) Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science, 279, 384-388. (Pubitemid 28063374)
29. Komatsu, H., Tsukahara, T. and Tozawa, H. (1996) Viral RNA binding properties of human immunodeficiency virus type-2 (HIV-2) nucleocapsid protein-derived synthetic peptides. Biochem. Mol. Biol. Int., 38, 1143-1154. (Pubitemid 26334728)
30. De Rocquigny, H., Gabus, C., Vincent, A., Fournie-Zaluski, M.C., Roques, B. and Darlix, J.L. (1992) Viral RNA annealing activities of human immunodeficiency virus type 1 nucleocapsid protein require only peptide domains outside the zinc fingers. Proc. Natl Acad. Sci. USA, 89, 6472-6476.
31. Oude Essink, B.B., Das, A.T. and Berkhout, B. (1996) HIV-1 reverse transcriptase discriminates against non-self tRNA primers. J. Mol. Biol., 264, 243-254. (Pubitemid 26402695)
32. Barik, S. (1997) Mutagenesis and gene fusion by megaprimer PCR. In White, B.A. (ed.), PCR Cloning Protocols. Humana Press, Totawa, NJ, pp. 173-182.
33. Pachulska-Wieczorek, K., Purzycka, K.J. and Adamiak, R.W. (2006) New, extended hairpin form of the TAR-2 RNA domain points to the structural polymorphism at the 5' end of the HIV-2 leader RNA. Nucleic Acids Res., 34, 2984-2997. (Pubitemid 44540426)
34. 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. USA, 101, 7287-7292. (Pubitemid 38638025)
35. Peattie, D.A. and Gilbert, W. (1980) Chemical probes for higher-order structure in RNA. Proc. Natl Acad. Sci. USA, 77, 4679-4682.
36. Ciesiolka, J., Michalowski, D., Wrzesinski, J., Krajewski, J. and Krzyzosiak, W.J. (1998) Patterns of cleavages induced by lead ions in defined RNA secondary structure motifs. J. Mol. Biol., 275, 211-220. (Pubitemid 28029999)
37. Krzyzosiak, W.J., Marciniec, T., Wiewiorowski, M., Romby, P., Ebel, J.P. and Giege, R. (1988) Characterization of the lead(II)-induced cleavages in tRNAs in solution and effect of the Y-base removal in yeast tRNAPhe. Biochemistry, 27, 5771-5777.
38. Wilkinson, K.A., Merino, E.J. and Weeks, K.M. (2006) Selective 2'-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat. Protoc., 1, 1610-1616.
39. Das, R., Laederach, A., Pearlman, S.M., Herschlag, D. and Altman, R.B. (2005) SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments. RNA, 11, 344-354. (Pubitemid 40270826)
40. Badorrek, C.S. and Weeks, K.M. (2006) Architecture of a gamma retroviral genomic RNA dimer. Biochemistry, 45, 12664-12672. (Pubitemid 44630851)
41. 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. (Pubitemid 40463047)
42. Gherghe, C., Leonard, C.W., Gorelick, R.J. and Weeks, K.M. (2010) Secondary structure of the mature ex virio Moloney murine leukemia virus genomic RNA dimerization domain. J. Virol., 84, 898-906.
43. Berkhout, B. (1992) Structural features in TAR RNA of human and simian immunodeficiency viruses: a phylogenetic analysis. Nucleic Acids Res., 20, 27-31.
44. Das, A.T., Klaver, B., Centlivre, M., Harwig, A., Ooms, M., Page, M., Almond, N., Yuan, F., Piatak, M. Jr, Lifson, J.D. et al. (2008) Optimization of the doxycycline-dependent simian immunodeficiency virus through in vitro evolution. Retrovirology, 5, 44.
45. Berkhout, B. and Schoneveld, I. (1993) Secondary structure of the HIV-2 leader RNA comprising the tRNA-primer binding site. Nucleic Acids Res., 21, 1171-1178. (Pubitemid 23155612)
46. Beltz, H., Azoulay, J., Bernacchi, S., Clamme, J.P., Ficheux, D., Roques, B., Darlix, J.L. and Mely, Y. (2003) Impact of the terminal bulges of HIV-1 cTAR DNA on its stability and the destabilizing activity of the nucleocapsid protein NCp7. J. Mol. Biol., 328, 95-108. (Pubitemid 36390283)
47. Williams, M.C., Rouzina, I., Wenner, J.R., Gorelick, R.J., Musier-Forsyth, K. and Bloomfield, V.A. (2001) Mechanism for nucleic acid chaperone activity of HIV-1 nucleocapsid protein revealed by single molecule stretching. Proc. Natl Acad. Sci. USA, 98, 6121-6126. (Pubitemid 32488203)
48. Huthoff, H. and Berkhout, B. (2001) Mutations in the TAR hairpin affect the equilibrium between alternative conformations of the HIV-1 leader RNA. Nucleic Acids Res., 29, 2594-2600. (Pubitemid 32600316)
49. Freund, F., Boulme, F., Litvak, S. and Tarrago-Litvak, L. (2001) Initiation of HIV-2 reverse transcription: a secondary structure model of the RNA-tRNA(Lys3) duplex. Nucleic Acids Res., 29, 2757-2765. (Pubitemid 32685038)
50. Matsui, T., Tanaka, T., Endoh, H., Sato, K., Tanaka, H., Miyauchi, E., Kawashima, Y., Nagai-Makabe, M., Komatsu, H., Kohno, T. et al. (2009) The RNA recognition mechanism of human immunodeficiency virus (HIV) type 2 NCp8 is different from that of HIV-1 NCp7. Biochemistry, 48, 4314-4323.
51. Fisher, R.J., Rein, A., Fivash, M., Urbaneja, M.A., Casas-Finet, J.R., Medaglia, M. and Henderson, L.E. (1998) Sequence-specific binding of human immunodeficiency virus type 1 nucleocapsid protein to short oligonucleotides. J. Virol., 72, 1902-1909. (Pubitemid 28100742)
52. Turner, K.B., Hagan, N.A. and Fabris, D. (2007) Understanding the isomerization of the HIV-1 dimerization initiation domain by the nucleocapsid protein. J. Mol. Biol., 369, 812-828. (Pubitemid 46709928)
53. Strong, C.L., Lanchy, J.M., Dieng-Sarr, A., Kanki, P.J. and Lodmell, J.S. (2009) A 5'UTR-spliced mRNA isoform is specialized for enhanced HIV-2 gag translation. J. Mol. Biol., 391, 426-437.
54. Berglund, J.A., Charpentier, B. and Rosbash, M. (1997) A high affinity binding site for the HIV-1 nucleocapsid protein. Nucleic Acids Res., 25, 1042-1049. (Pubitemid 27298275)