The human T-cell lymphotropic virus type-I dimerization initiation site forms a hairpin loop, unlike previously characterized retroviral dimerization motifs

Biochemistry

Volumn 43, Issue 20, 2004, Pages 6085-6090

  Monie, Tom P ^a,c   Greatorex, Jane S ^a   Zacharias, Martin ^b   Lever, Andrew M L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b JACOBS UNIVERSITY BREMEN   (Germany)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; DATA REDUCTION; DIMERIZATION; RNA; VIRUSES;

BIOCHEMICAL PROBING; MOLECULAR MODELING; STRUCTURAL MAP;

BIOCHEMISTRY;

CIS ACTING ELEMENT; DIMETHYL SULFATE; LEAD ACETATE; MONOMER; RIBONUCLEASE; RIBONUCLEASE T1; RIBONUCLEASE U2; RIBONUCLEASE V1; RNA; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; BASE PAIRING; DIMERIZATION; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR MODEL; MOLECULAR PROBE; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; RETROVIRUS; RNA SEQUENCE; RNA STRUCTURE; VIROGENESIS; VIRUS INFECTIVITY; VIRUS REPLICATION;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; DIMERIZATION; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RNA, VIRAL;

DELTARETROVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T-LYMPHOTROPIC VIRUS 1; RNA VIRUSES; UNIDENTIFIED RETROVIRUS;

EID: 2442636578     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi030237i     Document Type: Article

References (38)

1. 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.
2. Greatorex, J., and Lever, A. (1998) Retroviral RNA dimer linkage, J. Gen. Virol. 79, 2877-2882.
3. Berkhout, B., and van Wamel, J. L. B. (1996) Role of the DIS hairpin in replication of Human Immunodeficiency Virus Type 1, J. Virol. 70, 6723-6732.
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.
5. Paillart, J. C., Berthoux, L., Ottmann, M., Darlix, J. L., Marquet, R., Ehresmann, B., and 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.
6. Ly, H., Nierlich, D. P., Olsen, J. C., and Kaplan, A. H. (2000) Functional characterization of the dimer linkage structure RNA of Moloney murine sarcoma virus, J. Virol. 74, 9937-9945.
7. Mikkelsen, J. G., Lund, A. H., Duch, M., and Pedersen, F. S. (2000) Mutations of the kissing-loop dimerization sequence influence the site specificity of murine leukemia virus recombination in vivo, J. Virol. 74, 600-610.
8. Bieth, E., Gabus, C., and Darlix, J.-L. (1990) A study of the dimer formation of Rous sarcoma virus RNA and of its effect on viral protein synthesis in vitro, Nucleic Acids Res. 18, 119-127.
9. Clever, J. L., and Parslow, T. G. (1997) Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation, J. Virol. 71, 3407-3414.
10. Liang, C., Rong, L., Laughrea, M., Kleiman, L., and Wainberg, M. A. (1998) Compensatory point mutations in the human immunodeficiency virus type 1 gag region that are distal from deletion mutations in the dimerization initiation site can restore viral replication, J. Virol. 72, 6629-6636.
11. Liang, C., Rong, L., Quan, Y., Laughrea, M., Kleiman, L., and Wainberg, M. A. (1999) Mutations within four distinct gag proteins are required to restore replication of human immunodeficiency virus type 1 after deletion mutagenesis within the dimerization initiation site, J. Virol. 73, 7014-7020.
12. Ly, H., Nierlich, D. P., Olsen, J. C., and Kaplan, A. H. (1999) Moloney murine sarcoma virus genomic RNAs dimerize via a two-step process: a concentration-dependent kissing-loop interaction is driven by initial contact between consecutive guanines, J. Virol. 73, 7255-7261.
13. , Girard, P.-M., Bonnet-Mathoniere, B., Muriaux, D., and Paoletti, J. (1995) A short autocomplementary sequence in the 5′ leader region is responsible for dimerization of MoMuLV genomic RNA, Biochemistry 34, 9785-9794.
14. Laughrea, M., and Jette, L. (1996) Kissing-Loop Model Of HIV-1 Genome Dimerization-HIV-1 RNAs Can Assume Alternative Dimeric Forms, and All Sequences Upstream or Downstream Of Hairpin 248-271 Are Dispensable For Dimer Formation, Biochemistry 35, 1589-1598.
15. Paillart, J. C., Skripkin, E., Ehresmann, B., Ehresmann, C., and Marquet, R. (1996) A loop-loop "kissing" complex is the essential part of the dimer linkage of genomic HIV-1 RNA, Proc. Natl. Acad. Sci. U.S.A. 93, 5572-5577.
16. 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. U.S.A. 91, 4945-4949.
17. Greatorex, J. S., Laisse, V., Dokhelar, M.-C., and Lever, A. M. L. (1996) Sequences involved in the dimerisation of human T-cell leukaemia virus type-1 RNA, Nucleic Acids Res. 24, 2919-2923.
18. Le Blanc, I., Greatorex, J., Dokhelar M.-C., and Lever, A. M. L. (2000) A 37 base sequence in the leader region of human T-cell leukaemia virus type 1 is a high affinity dimerization site but is not essential for virus replication, J. Gen. Virol. 81, 105-108.
19. Monie, T., Greatorex, J., and Lever, A. M. L. (2001) Oligonucleotide mapping of the core dimer linkage in HTLV-1, Virus Res. 78, 45-56.
20. Klinck, R., Westhof, E., Walker, S., Afshar, M., Collier, A., and Aboul-Ela, F. (2000) A potential RNA drug target in the hepatitis C virus internal ribosomal entry site, RNA 6, 1423-1431.
21. Kim, C. H., Kao, C. C., and Tinoco, I., Jr. (2000) RNA motifs that determine specificity between a viral replicase and its promoter, Nat. Struct. Biol. 7, 415-423.
22. Battiste, J. L., Mao, H., Rao, N. S., Tan, R., Muhandiram, D. R., Kay, L. E., Frankel, A. D., and Williamson, J. R. (1996) Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex, Science 273, 1547-1551.
23. Joost Haasnoot, P. C., Olsthoorn, R. C., and Bol, J. F. (2002) The Brome mosaic virus subgenomic promoter hairpin is structurally similar to the iron-responsive element and functionally equivalent to the minus-strand core promoter stem-loop C, RNA 8, 110-122.
24. Mujeeb, A., Clever, J. L., Billeci, T. M., James, T. L., and Parslow, T. G. (1998) Structure of the dimer initiation complex of HIV-1 genomic RNA, Nat. Struct. Biol. 5, 432-436.
25. Ennifar, E., Walter, P., Ehresmann, B., Ehresmann, C., and Dumas, P. (2001) Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site, Nat. Struct. Biol. 8, 1064-1068.
26. Harrison, G. P., Mayo, M. S., Hunter, E., and Lever, A. M. L. (1998) Pausing of reverse transcriptase on retroviral RNA templates is influenced by secondary structures both 5′ and 3′ of the catalytic site, Nucleic Acids Res. 26, 3433-3442.
27. Mathews, D. H., Sabina, J., Zuker, M., and Turner, D. H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure, J. Mol. Biol. 288, 911-940.
28. Zuker, M., Mathews, D. H., and Turner, D. H. (1999) in RNA Biochemistry and Biotechnology (Barciszewski, J., and Clark, B. F. C., Eds.) pp 11-43, NATO ASI Series, Kluwer Academic Publishers.
29. Lavery, R., Zakrzewska, K., and Sklenar, H. (1995) JUMNA (Junction Minimisation of Nucleic Acids), Comput. Phys. Commun. 91, 135-158.
30. Zacharias, M. (2001) Conformational analysis of DNA-trinucleotide-hairpin-loop structures using a continuum solvent model, Biophys. J. 80, 2350-2363.
31. Varani, G., Cheong, C., and Tinoco, I., Jr. (1991) Structure of an unusually stable RNA hairpin, Biochemistry 30, 3280-3289.
32. Ratner, L., Philpott, T., and Trowbridge, D. B. (1991) Nucleotide sequence analysis of isolates of human T-lymphotropic virus type 1 of diverse geographical origins, AIDS Res. Hum. Retroviruses 7, 923-941.
33. Ennifar, E., Yusupov, M., Walter, P., Marquet, R., Ehresmann, B., Ehresmann, C., and Dumas, P. (1999) The crystal structure of the dimerization initiation site of genomic HIV-1 RNA reveals an extended duplex with two adenine bulges, Struct. Fold. Des. 7, 1439-1449.
34. Kean, J. M., and Draper, D. E. (1985) Secondary structure of a 345-base RNA fragment covering the S8/S15 protein binding domain of Escherichia coli 16S ribosomal RNA, Biochemistry 24, 5052-5061.
35. 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.
36. 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.
37. Ly, H., and Parslow, T. G. (2002) Bipartite signal for genomic RNA dimerization in Moloney murine leukemia virus, J Virol. 76, 3135-3144.
38. 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.