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

Journal of Molecular Biology

Volumn 322, Issue 3, 2002, Pages 543-557

  Greatorex, Jane ^a   Gallego, José ^b   Varani, Gabriele ^b   Lever, Andrew ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Dimerisation; HIV; NMR; RNA; SL 1

Indexed keywords

GAG PROTEIN; GENOMIC RNA; MESSENGER RNA; NUCLEOTIDE; PURINE; REV PROTEIN;

ARTICLE; BINDING SITE; CONFORMATION; DIMERIZATION; DNA RESPONSIVE ELEMENT; HUMAN IMMUNODEFICIENCY VIRUS 1; MELTING POINT; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYLOGENY; PRIORITY JOURNAL; PROTEIN STRUCTURE; RNA ANALYSIS; RNA SPLICING; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; THERMODYNAMICS; ULTRAVIOLET RADIATION; WILD TYPE;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0036385821     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)00776-3     Document Type: Article

References (51)

1. Berkowitz, R., Fisher, J. & Goff, S. P. (1996). RNA packaging. Curr. Top. Microbiol. Immunol. 214, 177-218.
2. Jewell, A. N. & Mansky, L. M. (2000). In the beginning: genome recognition, RNA encapsidation and the initiation of complex retrovirus assembly. J. Gen. Virol. 81, 1889-1899.
3. Pappalardo, L., Kerwood, D. J., Pelczer, I. & Borer, P. N. (1998). Three-dimensional folding of an RNA hairpin required for packaging HIV-1. J. Mol. Biol. 282, 801-818.
4. Zeffman, A., Hassard, S., Varani, G. & Lever, A. (2000). The major HIV-1 packaging signal is an extended bulged stem-loop whose structure is altered on interaction with the Gag polyprotein. J. Mol. Biol. 297, 877-893.
5. De Guzman, R. N., Wu, Z. R., Stalling, C. C., Pappalardo, L., Borer, P. N. & Summers, M. F. (1998). Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science, 279, 384-388.
6. Amarasinghe, G. K., De Guzman, R. N., Turner, R. B. & Summers, M. F. (2000). NMR structure of stem-loop SL2 of the HIV-1 psi RNA packaging signal reveals a novel A-U-A base-triple platform. J. Mol. Biol. 299, 145-156.
7. Amarasinghe, G. K., De Guzman, R. N., Turner, R. B., Chancellor, K. J., Wu, Z. R. & Summers, M. F. (2000). NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the psi-RNA packaging signal. Implications for genome recognition. J. Mol. Biol. 301, 491-511.
8. Amarasinghe, G. K., Zhou, J., Miskimon, M., Chancellor, K. J., McDonald, J. A., Matthews, A. G. et al. (2001). Stem-loop SL4 of the HIV-1 psi RNA packaging signal exhibits weak affinity for the nucleocapsid protein. Structural studies and implications for genome recognition. J. Mol. Biol. 314, 961-970.
9. Kerwood, D. J., Cavaluzzi, M. J. & Borer, P. N. (2001). Structure of SL4 RNA from the HIV-1 packaging signal. Biochemistry, 40, 14518-14529.
10. Greatorex, J. & Lever, A. (1998). Retroviral RNA dimer linkage. J. Gen. Virol. 79, 2877-2882.
11. Skripkin, E., Paillart, J. C., Marquet, R., Ehresmann, B. & 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.
12. Paillart, J. C., Westhof, E., Ehresmann, C., Ehresmann, B. & Marquet, R. (1997). Non-canonical interactions in a kissing loop complex: the dimerization initiation site of HIV-1 genomic RNA. J. Mol. Biol. 270, 36-49.
13. Laughrea, M. & Jette, L. (1994). A 19-nucleotide sequence upstream of the 5′ major splice donor is part of the dimerization domain of human immunodeficiency virus 1 genomic RNA. Biochemistry, 33, 13464-13474.
14. Laughrea, M., Jette, L., Mak, J., Kleiman, L., Liang, C. & Wainberg, M. A. (1997). Mutations in the kissing-loop hairpin of human immunodeficiency virus type 1 reduce viral infectivity as well as genomic RNA packaging and dimerization. J. Virol. 71, 3397-3406.
15. Paillart, J. C., Berthoux, L., Ottmann, M., Darlix, J. L., Marquet, R., Ehresmann, B. & Ehresmann, C. (1996). A dual role of the putative RNA dimerization initiation site of human immunodeficiency virus type 1 in genomic RNA packaging and proviral DNA synthesis. J. Virol. 70, 8348-8354.
16. Berkhout, B. & van Wamel, J. L. (1996). Role of the DIS hairpin in replication of human immunodeficiency virus type 1. J. Virol. 70, 6723-6732.
17. Clever, J. L. & Parslow, T. G. (1997). Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation. J. Virol. 71, 3407-3414.
18. Balakrishnan, M., Fay, P. J. & Bambara, R. A. (2001). The kissing hairpin sequence promotes recombination within the HIV-I 5′ leader region. J. Biol. Chem. 276, 36482-36492.
19. Mujeeb, A., Clever, J. L., Billeci, T. M., James, T. L. & Parslow, T. G. (1998). Structure of the dimer initiation complex of HIV-1 genomic RNA. Nature Struct. Biol. 5, 432-436.
20. Girard, F., Barbault, F., Gouyette, C., Huynh-Dinh, T., Paoletti, J. & Lancelot, G. (1999). Dimer initiation sequence of HIV-1Lai genomic RNA: NMR solution structure of the extended duplex. J. Biomol. Struct. Dynam. 16, 1145-1157.
21. Mujeeb, A., Parslow, T. G., Zarrinpar, A., Das, C. & James, T. L. (1999). NMR structure of the mature dimer initiation complex of HIV-1 genomic RNA. FEBS Letters, 458, 387-392.
22. Ennifar, E., Walter, P., Ehresmann, B., Ehresmann, C. & Dumas, P. (2001). Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site. Nature Struct. Biol. 8, 1064-1068.
23. Harrison, G. P., Miele, G., Hunter, E. & Lever, A. M. L. (1998). Functional analysis of the core human immunodeficiency virus type 1 packaging signal in a permissive cell line. J. Virol. 72, 5886-5896.
24. Takahashi, K. I., Baba, S., Chattopadhyay, P., Koyanagi, Y., Yamamoto, N., Takaku, H. & Kawai, G. (2000). Structural requirement for the two-step dimerization of human immunodeficiency virus type 1 genome. RNA, 6, 96-102.
25. Takahashi, K., Baba, S., Hayashi, Y., Koyanagi, Y., Yamamoto, N., Takaku, H. & Kawai, G. (2000). NMR analysis of intra- and inter-molecular stems in the dimerization initiation site of the HIV-1 genome. J. Biochem. (Tokyo), 127, 681-686.
26. Allain, F. H. & Varani, G. (1995). Structure of the P1 helix from group I self-splicing introns. J. Mol. Biol. 250, 333-353.
27. Collier, A., Gallego, J., Klinck, R., Cole, P. T., Harris, S. J., Harrison, G. et al. (2002). A conserved RNA structure within the HCV IRES eIF3 binding site. Nature Struct. Biol. 9, 375-380.
28. Szewczak, A. A., Moore, P. B., Chang, Y. L. & Wool, I. G. (1993). The conformation of the sarcin/ricin loop from 28 S ribosomal RNA. Proc. Natl Acad. Sci. USA, 90, 9581-9585.
29. Wimberly, B., Varani, G. & Tinoco, I., Jr (1993). The conformation of loop E of eukaryotic 5 S ribosomal RNA. Biochemistry, 32, 1078-1087.
30. Elgavish, T., Cannone, J. J., Lee, J. C., Harvey, S. C. & Gutell, R. R. (2001). AA.AG@helix.ends: A:A and A:G base-pairs at the ends of 16 S and 23 S rRNA helices. J. Mol. Biol. 310, 735-753.
31. Battiste, J. L., Mao, H., Rao, N. S., Tan, R., Muhandiram, D. R., Kay, L. E. et al. (1996). Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex. Science, 273, 1547-1551.
32. Peterson, R. D., Bartel, D. P., Szostak, J. W., Horvath, S. J. & Feigon, J. (1994). 1H NMR studies of the high--affinity Rev binding site of the Rev responsive element of HIV-1 mRNA: base pairing in the core binding element. Biochemistry, 33, 5357-5366.
33. Peterson, R. D. & Feigon, J. (1996). Structural change in Rev responsive element RNA of HIV-1 on binding Rev peptide. J. Mol. Biol. 264, 863-877.
34. Hung, L. W., Holbrook, E. L. & Holbrook, S. R. (2000). The crystal structure of the Rev binding element of HIV-1 reveals novel base pairing and conformational variability. Proc. Natl Acad. Sci. USA, 97, 5107-5112.
35. SantaLucia, J., Jr & Turner, D. H. (1993). Structure of (rGGCGAGCC)2 in solution from NMR and restrained molecular dynamics. Biochemistry, 32, 12612-12623.
36. Dallas, A. & Moore, P. B. (1997). The loop E-loop D region of Escherichia coli 5 S rRNA: the solution structure reveals an unusual loop that may be important for binding ribosomal proteins. Structure, 5, 1639-1653.
37. Sizova, D., Kolupaeva, V., Pestova, T., Shatsky, I. & Hellen, C. (1998). Specific interaction of eukaryotic translation initiation factor 3 with the 5′ nontranslated regions of hepatitis C virus and classical swine fever virus RNAs. J. Virol. 72, 4775-4782.
38. Burkard, M. & Turner, D. (2000). NMR structures of r(GCAGGCGUGC)2 and determinants of stability for single guanosine-guanosine base pairs. Biochemistry, 39, 11748-11762.
39. Rein, A., Henderson, L. E. & Levin, J. G. (1998). Nucleic-acid-chaperone activity of retroviral nucleo-capsid proteins: significance for viral replication. Trends Biochem. Sci. 23, 297-301.
40. Darlix, J. L., Lapadat-Tapolsky, M., de Rocquigny, H. & Roques, B. P. (1995). First glimpses at structure-function relationships of the nucleocapsid protein of retroviruses. J. Mol. Biol. 254, 523-537.
41. Feng, Y. X., Copeland, T. D., Henderson, L. E., Gorelick, R. J., Bosche, W. J., Levin, J. G. & Rein, A. (1996). HIV-1 nucleocapsid protein induces "maturation" of dimeric retroviral RNA in vitro. Proc. Natl Acad. Sci. USA, 93, 7577-7581.
42. Feng, Y. X., Campbell, S., Harvin, D., Ehresmann, B., Ehresmann, C. & Rein, A. (1999). The human immunodeficiency virus type 1 Gag polyprotein has nucleic acid chaperone activity: possible role in dimerization of genomic RNA and placement of tRNA on the primer binding site. J. Virol. 73, 4251-4256.
43. Harrison, G. P. & Lever, A. M. (1992). The human immunodeficiency virus type 1 packaging signal and major splice donor region have a conserved stable secondary structure. J. Virol. 66, 4144-4153.
44. Clever, J., Sassetti, C. & Parslow, T. G. (1995). RNA secondary structure and binding sites for gag gene products in the 5′ packaging signal of human immunodeficiency virus type 1. J. Virol. 69, 2101-2109.
45. Kieft, J. S., Zhou, K., Jubin, R. & Doudna, J. A. (2001). Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA, 7, 194-206.
46. Richardson, J. H., Child, L. A. & Lever, A. M. (1993). Packaging of human immunodeficiency virus type 1 RNA requires cis-acting sequences outside the 5′ leader region. J. Virol. 67, 3997-4005.
47. Huthoff, H. & Berkhout, B. (2001). Two alternating structures of the HIV-1 leader RNA. RNA, 7, 143-157.
48. Damgaard, C. K., Dyhr-Mikkelsen, H. & 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. Nucl. Acids Res. 26, 3667-3676.
49. Price, S. R., Evans, P. R. & Nagai, K. (1998). Crystal structure of the spliceosomal U2B″-U2A′ protein complex bound to a fragment of U2 small nuclear RNA. Nature, 394, 645-650.
50. Kao, C., Zheng, M. & Rudisser, S. (1999). A simple and efficient method to reduce nontemplated nucleotide addition at the 3 terminus of RNAs transcribed by T7 RNA polymerase. RNA, 5, 1268-1272.
51. Brunger, A. T. (1996). X-PLOR Manual, Yale University, New Haven, CT.