The Interaction between tRNALys3 and the Primer Activation Signal Deciphered by NMR Spectroscopy

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Sleiman, Dona ^a   Barraud, Pierre ^a   Brachet, Franck ^a   Tisne, Carine ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE TRANSFER RNA; NUCLEOCAPSID PROTEIN; 5' UNTRANSLATED REGION; PRIMER DNA; VIRUS RNA;

ARTICLE; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; PRIMER ACTIVATION SIGNAL; PRIMER BINDING SITE; REVERSE TRANSCRIPTION; RNA STRUCTURE; VIRUS GENOME; 5' UNTRANSLATED REGION; BASE PAIRING; BINDING SITE; CONFORMATION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; MOLECULAR GENETICS; VIROLOGY; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

5' UNTRANSLATED REGIONS; BASE PAIRING; BASE SEQUENCE; BINDING SITES; DNA PRIMERS; GENE EXPRESSION REGULATION; GENOME, VIRAL; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; NUCLEOCAPSID PROTEINS; REVERSE TRANSCRIPTION; RNA, TRANSFER, LYS; RNA, VIRAL; VIRUS REPLICATION;

EID: 84878807377     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064700     Document Type: Article

References (58)

1. Marquet R, Isel C, Ehresmann C, Ehresmann B, (1995) tRNAs as primer of reverse transcriptases. Biochimie 77: 113-124.
2. Mak J, Kleiman L, (1997) Primer tRNAs for reverse transcription. J Virol 71: 8087-8095.
3. Darlix JL, Cristofari G, Rau M, Pechoux C, Berthoux L, et al. (2000) Nucleocapsid protein of human immunodeficiency virus as a model protein with chaperoning functions and as a target for antiviral drugs. Advances in pharmacology 48: 345-372.
4. Levin JG, Mitra M, Mascarenhas A, Musier-Forsyth K, (2010) Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription. RNA Biol 7: 754-774.
5. Tisne C, (2005) Structural bases of the annealing of primer tRNA(3Lys) to the HIV-1 viral RNA. Current HIV research 3: 147-156.
6. Tisne C, Roques BP, Dardel F, (2001) Heteronuclear NMR studies of the interaction of tRNA(Lys)3 with HIV-1 nucleocapsid protein. J Mol Biol 306: 443-454.
7. Tisne C, Roques BP, Dardel F, (2004) The annealing mechanism of HIV-1 reverse transcription primer onto the viral genome. J Biol Chem 279: 3588-3595.
8. Hargittai MR, Gorelick RJ, Rouzina I, Musier-Forsyth K, (2004) Mechanistic insights into the kinetics of HIV-1 nucleocapsid protein-facilitated tRNA annealing to the primer binding site. J Mol Biol 337: 951-968.
9. Barraud P, Gaudin C, Dardel F, Tisne C, (2007) New insights into the formation of HIV-1 reverse transcription initiation complex. Biochimie 89: 1204-1210.
10. Li X, Mak J, Arts EJ, Gu Z, Kleiman L, et al. (1994) Effects of alterations of primer-binding site sequences on human immunodeficiency virus type 1 replication. J Virol 68: 6198-6206.
11. Das AT, Brummelkamp TR, Westerhout EM, Vink M, Madiredjo M, et al. (2004) Human immunodeficiency virus type 1 escapes from RNA interference-mediated inhibition. J Virol 78: 2601-2605.
12. Wakefield JK, Wolf AG, Morrow CD, (1995) Human immunodeficiency virus type 1 can use different tRNAs as primers for reverse transcription but selectively maintains a primer binding site complementary to tRNA(3Lys). J Virol 69: 6021-6029.
13. Barat C, Lullien V, Schatz O, Keith G, Nugeyre MT, et al. (1989) HIV-1 reverse transcriptase specifically interacts with the anticodon domain of its cognate primer tRNA. The EMBO journal 8: 3279-3285.
14. Abbink TE, Beerens N, Berkhout B, (2004) Forced selection of a human immunodeficiency virus type 1 variant that uses a non-self tRNA primer for reverse transcription: involvement of viral RNA sequences and the reverse transcriptase enzyme. J Virol 78: 10706-10714.
15. Abbink TE, Berkhout B, (2007) HIV-1 reverse transcription: close encounters between the viral genome and a cellular tRNA. Advances in pharmacology 55: 99-135.
16. Beerens N, Berkhout B, (2002) Switching the in vitro tRNA usage of HIV-1 by simultaneous adaptation of the PBS and PAS. RNA 8: 357-369.
17. Beerens N, Berkhout B, (2002) The tRNA primer activation signal in the human immunodeficiency virus type 1 genome is important for initiation and processive elongation of reverse transcription. J Virol 76: 2329-2339.
18. Beerens N, Groot F, Berkhout B, (2001) Initiation of HIV-1 reverse transcription is regulated by a primer activation signal. J Biol Chem 276: 31247-31256.
19. Dupuy LC, Kelly NJ, Elgavish TE, Harvey SC, Morrow CD, (2003) Probing the importance of tRNA anticodon: human immunodeficiency virus type 1 (HIV-1) RNA genome complementarity with an HIV-1 that selects tRNA(Glu) for replication. J Virol 77: 8756-8764.
20. Isel C, Ehresmann C, Keith G, Ehresmann B, Marquet R, (1995) Initiation of reverse transcription of HIV-1: secondary structure of the HIV-1 RNA/tRNA(3Lys) (template/primer). J Mol Biol 247: 236-250.
21. Isel C, Marquet R, Keith G, Ehresmann C, Ehresmann B, (1993) Modified nucleotides of tRNA(3Lys) modulate primer/template loop-loop interaction in the initiation complex of HIV-1 reverse transcription. J Biol Chem 268: 25269-25272.
22. Isel C, Westhof E, Massire C, Le Grice SF, Ehresmann B, et al. (1999) Structural basis for the specificity of the initiation of HIV-1 reverse transcription. Embo J 18: 1038-1048.
23. Iwatani Y, Rosen AE, Guo J, Musier-Forsyth K, Levin JG, (2003) Efficient initiation of HIV-1 reverse transcription in vitro. Requirement for RNA sequences downstream of the primer binding site abrogated by nucleocapsid protein-dependent primer-template interactions. J Biol Chem 278: 14185-14195.
24. Kang SM, Zhang Z, Morrow CD, (1997) Identification of a sequence within U5 required for human immunodeficiency virus type 1 to stably maintain a primer binding site complementary to tRNA(Met). J Virol 71: 207-217.
25. Kang SM, Zhang Z, Morrow CD, (1999) Identification of a human immunodeficiency virus type 1 that stably uses tRNALys1,2 rather than tRNALys,3 for initiation of reverse transcription. Virology 257: 95-105.
26. Wakefield JK, Kang SM, Morrow CD, (1996) Construction of a type 1 human immunodeficiency virus that maintains a primer binding site complementary to tRNA(His). J Virol 70: 966-975.
27. Zhang Z, Kang SM, LeBlanc A, Hajduk SL, Morrow CD, (1996) Nucleotide sequences within the U5 region of the viral RNA genome are the major determinants for an human immunodeficiency virus type 1 to maintain a primer binding site complementary to tRNA(His). Virology 226: 306-317.
28. Aiyar A, Cobrinik D, Ge Z, Kung HJ, Leis J, (1992) Interaction between retroviral U5 RNA and the T psi C loop of the tRNA(Trp) primer is required for efficient initiation of reverse transcription. J Virol 66: 2464-2472.
29. Liang C, Li X, Rong L, Inouye P, Quan Y, et al. (1997) The importance of the A-rich loop in human immunodeficiency virus type 1 reverse transcription and infectivity. J Virol 71: 5750-5757.
30. Miller JT, Ehresmann B, Hubscher U, Le Grice SF, (2001) A novel interaction of tRNA(Lys,3) with the feline immunodeficiency virus RNA genome governs initiation of minus strand DNA synthesis. J Biol Chem 276: 27721-27730.
31. Sleiman D, Goldschmidt V, Barraud P, Marquet R, Paillart JC, et al. (2012) Initiation of HIV-1 reverse transcription and functional role of nucleocapsid-mediated tRNA/viral genome interactions. Virus research 169: 324-339.
32. Goldschmidt V, Ehresmann C, Ehresmann B, Marquet R, (2003) Does the HIV-1 primer activation signal interact with tRNA3(Lys) during the initiation of reverse transcription? Nucleic Acids Res 31: 850-859.
33. Goldschmidt V, Paillart JC, Rigourd M, Ehresmann B, Aubertin AM, et al. (2004) Structural variability of the initiation complex of HIV-1 reverse transcription. J Biol Chem 279: 35923-35931.
34. Freund F, Boulme F, Litvak S, 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.
35. Beerens N, Jepsen MD, Nechyporuk-Zloy V, Kruger AC, Darlix JL, et al. (2013) Role of the primer activation signal in tRNA annealing onto the HIV-1 genome studied by single-molecule FRET microscopy. RNA.
36. Pervushin K, Riek R, Wider G, Wuthrich K, (1997) Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci U S A 94: 12366-12371.
37. Weigelt J, (1998) Single scan, sensitivity- and gradient-enhanced TROSY for multidimensional NMR experiments. J Am Chem Soc 120: 10778-10779.
38. Puglisi EV, Puglisi JD, (2011) Secondary structure of the HIV reverse transcription initiation complex by NMR. J Mol Biol 410: 863-874.
39. Tisne C, Rigourd M, Marquet R, Ehresmann C, Dardel F, (2000) NMR and biochemical characterization of recombinant human tRNA(Lys)3 expressed in Escherichia coli: identification of posttranscriptional nucleotide modifications required for efficient initiation of HIV-1 reverse transcription. RNA 6: 1403-1412.
40. Baudin F, Marquet R, Isel C, Darlix JL, Ehresmann B, et al. (1993) Functional sites in the 5′ region of human immunodeficiency virus type 1 RNA form defined structural domains. J Mol Biol 229: 382-397.
41. Berkhout B, (1996) Structure and function of the human immunodeficiency virus leader RNA. Prog Nucleic Acid Res Mol Biol 54: 1-34.
42. Cruceanu M, Urbaneja MA, Hixson CV, Johnson DG, Datta SA, et al. (2006) Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins. Nucleic Acids Res 34: 593-605.
43. Levin JG, Guo J, Rouzina I, Musier-Forsyth K, (2005) Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog Nucleic Acid Res Mol Biol 80: 217-286.
44. Rein A, Henderson LE, Levin JG, (1998) Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem Sci 23: 297-301.
45. Abbink TE, Berkhout B, (2008) HIV-1 reverse transcription initiation: a potential target for novel antivirals? Virus research 134: 4-18.
46. Azoulay J, Clamme JP, Darlix JL, Roques BP, Mely Y, (2003) Destabilization of the HIV-1 complementary sequence of TAR by the nucleocapsid protein through activation of conformational fluctuations. J Mol Biol 326: 691-700.
47. Beltz H, Piemont E, Schaub E, Ficheux D, Roques B, et al. (2004) Role of the structure of the top half of HIV-1 cTAR DNA on the nucleic acid destabilizing activity of the nucleocapsid protein NCp7. J Mol Biol 338: 711-723.
48. Cruceanu M, Gorelick RJ, Musier-Forsyth K, Rouzina I, Williams MC, (2006) Rapid kinetics of protein-nucleic acid interaction is a major component of HIV-1 nucleocapsid protein's nucleic acid chaperone function. J Mol Biol 363: 867-877.
49. Williams MC, Rouzina I, Wenner JR, Gorelick RJ, Musier-Forsyth K, et al. (2001) Mechanism for nucleic acid chaperone activity of HIV-1 nucleocapsid protein revealed by single molecule stretching. Proc Natl Acad Sci U S A 98: 6121-6126.
50. Ooms M, Cupac D, Abbink TE, Huthoff H, Berkhout B, (2007) The availability of the primer activation signal (PAS) affects the efficiency of HIV-1 reverse transcription initiation. Nucleic Acids Res 35: 1649-1659.
51. Isel C, Keith G, Ehresmann B, Ehresmann C, Marquet R, (1998) Mutational analysis of the tRNA3Lys/HIV-1 RNA (primer/template) complex. Nucleic Acids Res 26: 1198-1204.
52. Houzet L, Morichaud Z, Didierlaurent L, Muriaux D, Darlix JL, et al. (2008) Nucleocapsid mutations turn HIV-1 into a DNA-containing virus. Nucleic acids research 36: 2311-2319.
53. Saadatmand J, Niu M, Kleiman L, Guo F, (2009) The contribution of the primer activation signal to differences between Gag- and NCp7-facilitated tRNA(Lys3) annealing in HIV-1. Virology 391: 334-341.
54. Cen S, Khorchid A, Gabor J, Rong L, Wainberg MA, et al. (2000) Roles of Pr55(gag) and NCp7 in tRNA(3)(Lys) genomic placement and the initiation step of reverse transcription in human immunodeficiency virus type 1. J Virol 74: 10796-10800.
55. Lee BM, De Guzman RN, Turner BG, Tjandra N, Summers MF, (1998) Dynamical behavior of the HIV-1 nucleocapsid protein. J Mol Biol 279: 633-649.
56. De Guzman RN, Wu ZR, Stalling CC, Pappalardo L, Borer PN, et al. (1998) Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science 279: 384-388.
57. Markham NR, Zuker M, (2005) DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res 33: W577-581.
58. Piotto M, Saudek V, Sklenar V, (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR 2: 661-665.