Characterization of the inhibition mechanism of HIV-1 nucleocapsid protein chaperone activities by methylated oligoribonucleotides

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 2, 2012, Pages 1010-1018

  Avilov, Sergiy V ^a,c   Boudier, Christian ^a   Gottikh, Marina ^b   Darlix, Jean Luc ^a   Mély, Yves ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; COMPLEMENTARY DNA; METHYLATED OLIGORIBONUCLEOTIDE; NUCLEIC ACID; NUCLEOCAPSID PROTEIN; OLIGORIBONUCLEOTIDE; RNA DIRECTED DNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS DNA; ZINC FINGER PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; DNA SYNTHESIS; FLUORESCENCE; FLUORESCENCE ANALYSIS; HUMAN IMMUNODEFICIENCY VIRUS 1; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS NUCLEOCAPSID;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA, VIRAL; HIV REVERSE TRANSCRIPTASE; HIV-1; HUMANS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; NUCLEOCAPSID PROTEINS; OLIGORIBONUCLEOTIDES;

EID: 84856072897     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.05614-11     Document Type: Article

References (46)

1. Amarasinghe GK, et al. 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.
2. Avilov SV, Godet J, Piemont E, Mely Y. 2009. Site-specific characterization of HIV-1 nucleocapsid protein binding to oligonucleotides with two binding sites. Biochemistry 48:2422-2430.
3. Avilov SV, Piemont E, Shvadchak V, de Rocquigny H, Mely Y. 2008. Probing dynamics of HIV-1 nucleocapsid protein/target hexanucleotide complexes by 2-aminopurine. Nucleic Acids Res. 36:885-896. (Pubitemid 351267244)
4. Beltz H, et al. 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)
5. Beltz H, et al. 2005. Structural determinants of HIV-1 nucleocapsid protein for cTAR DNA binding and destabilization, and correlation with inhibition of self-primed DNA synthesis. J. Mol. Biol. 348:1113-1126. (Pubitemid 40602370)
6. Beltz H, 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. (Pubitemid 38507416)
7. Bernacchi S, Piemont E, Potier N, Dorsselaer A, Mely Y. 2003. Excitonic heterodimer formation in an HIV-1 oligonucleotide labeled with a donoracceptor pair used for fluorescence resonance energy transfer. Biophys. J. 84:643-654. (Pubitemid 36026432)
8. Bernacchi S, et al. 2002. HIV-1 nucleocapsid protein activates transient melting of least stable parts of the secondary structure of TAR and its complementary sequence. J. Mol. Biol. 317:385-399. (Pubitemid 34722178)
9. Bombarda E, et al. 1999. Time-resolved fluorescence investigation of the human immunodeficiency virus type 1 nucleocapsid protein: influence of the binding of nucleic acids. Biophys. J. 76:1561-1570. (Pubitemid 29262634)
10. Bourbigot S, et al. 2008. How the HIV-1 nucleocapsid protein binds and destabilises the (-)primer binding site during reverse transcription. J. Mol. Biol. 383:1112-1128.
11. Buckman JS, Bosche WJ, Gorelick RJ. 2003. Human immunodeficiency virus type 1 nucleocapsid Zn(2+) fingers are required for efficient reverse transcription, initial integration processes, and protection of newly synthesized viral DNA. J. Virol. 77:1469-1480. (Pubitemid 36055568)
12. Clever J, Sassetti C, Parslow TG. 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.
13. Darlix JL, et al. 2011. Flexible nature and specific functions of the HIV-1 nucleocapsid protein. J. Mol. Biol. 410:565-581.
14. De Guzman RN, et al. 1998. Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science 279:384-388. (Pubitemid 28063374)
15. de Rocquigny H, et al. 1991. First large scale chemical synthesis of the 72 amino acid HIV-1 nucleocapsid protein NCp7 in an active form. Biochem. Biophys. Res. Commun. 180:1010-1018.
16. de Rocquigny H, et al. 2008. Targeting the viral nucleocapsid protein in anti-HIV-1 therapy. Mini Rev. Med. Chem. 8:24-35. (Pubitemid 351320927)
17. Dorfman T, Luban J, Goff SP, Haseltine WA, Gottlinger HG. 1993. Mapping of functionally important residues of a cysteine-histidine box in the human immunodeficiency virus type 1 nucleocapsid protein. J. Virol. 67:6159-6169. (Pubitemid 23277528)
18. Driscoll MD, Hughes SH. 2000. Human immunodeficiency virus type 1 nucleocapsid protein can prevent self-priming of minus-strand strong stopDNAby promoting the annealing of short oligonucleotides to hairpin sequences. J. Virol. 74:8785-8792.
19. Druillennec S, Caneparo A, de Rocquigny H, Roques BP. 1999. Evidence of interactions between the nucleocapsid protein NCp7 and the reverse transcriptase of HIV-1. J. Biol. Chem. 274:11283-11288.
20. Egele C, et al. 2004. HIV-1 nucleocapsid protein binds to the viral DNA initiation sequences and chaperones their kissing interactions. J. Mol. Biol. 342:453-466. (Pubitemid 39149750)
21. Fisher RJ, et al. 2006. Complex interactions of HIV-1 nucleocapsid protein with oligonucleotides. Nucleic Acids Res. 34:472-484. (Pubitemid 43240237)
22. Fisher RJ, et al. 1998. Sequence-specific binding of human immunodeficiency virus type 1 nucleocapsid protein to short oligonucleotides. J. Virol. 72:1902-1909. (Pubitemid 28100742)
23. Godet J, et al. 2006. During the early phase of HIV-1 DNA synthesis, nucleocapsid protein directs hybridization of the TAR complementary sequences via the ends of their double-stranded stem. J. Mol. Biol. 356:1180-1192. (Pubitemid 43199922)
24. Godet J, Mely Y. 2010. Biophysical studies of the nucleic acid chaperone properties of the HIV-1 nucleocapsid protein. RNA Biol. 7:687-699.
25. Godet J, et al. 2011. Specific implications of the HIV-1 nucleocapsid zinc fingers in the annealing of the primer binding site complementary sequences during the obligatory plus strand transfer. Nucleic Acids Res. 39:6633-6645.
26. Goldschmidt V, Miller Jenkins LM, De Rocquigny H, Darlix JL, Mely Y. 2010. The nucleocapsid protein of HIV-1 as a promising therapeutic target for antiviral drugs. HIV Ther. 4:179-198.
27. Golinelli MP, Hughes SH. 2003. Secondary structure in the nucleic acid affects the rate of HIV-1 nucleocapsid-mediated strand annealing. Biochemistry 42:8153-8162. (Pubitemid 36858976)
28. Grigorov B, et al. 2011. Identification of a methylated oligoribonucleotide as a potent inhibitor of HIV-1 reverse transcription complex. Nucleic Acids Res. 39:5586-5596.
29. Grohmann D, Godet J, Mely Y, Darlix JL, Restle T. 2008. HIV-1 nucleocapsid traps reverse transcriptase on nucleic acid substrates. Biochemistry 47:12230-12240.
30. Guo J, Henderson LE, Bess J, Kane B, Levin JG. 1997. Human immunodeficiency virus type 1 nucleocapsid protein promotes efficient strand transfer and specific viral DNA synthesis by inhibiting TAR-dependent self-priming from minus-strand strong-stop DNA. J. Virol. 71:5178-5188. (Pubitemid 27258190)
31. Guo J, et al. 2000. Zinc finger structures in the human immunodeficiency virus type 1 nucleocapsid protein facilitate efficient minus-and plusstrand transfer. J. Virol. 74:8980-8988.
32. Heilman-Miller SL, Wu T, Levin JG. 2004. Alteration of nucleic acid structure and stability modulates the efficiency of minus-strand transfer mediated by the HIV-1 nucleocapsid protein. J. Biol. Chem. 279:44154-44165. (Pubitemid 39390723)
33. Korolev S, et al. 2011. Modulation of HIV-1 integrase activity by single-stranded oligonucleotides and their conjugates with eosin. Nucleosides Nucleotides Nucleic Acids 30:651-666.
34. Lakowitz JR. 1999. Principles of fluorescence spectroscopy, 2nd ed. Springer, New York, NY.
35. Lapadat-Tapolsky M, Gabus C, Rau M, Darlix JL. 1997. Possible roles of HIV-1 nucleocapsid protein in the specificity of proviral DNA synthesis and in its variability. J. Mol. Biol. 268:250-260. (Pubitemid 27208052)
36. 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. (Pubitemid 43574891)
37. Mihailescu MR, Marino JP. 2004. A proton-coupled dynamic conformational switch in the HIV-1 dimerization initiation site kissing complex. Proc. Natl. Acad. Sci. U. S. A. 101:1189-1194. (Pubitemid 38182664)
38. Record MT, Jr, Lohman ML, De Haseth P. 1976. Ion effects on ligandnucleic acid interactions. J. Mol. Biol. 107:145-158.
39. Spolar RS, Record MT, Jr. 1994. Coupling of local folding to site-specific binding of proteins to DNA. Science 263:777-784. (Pubitemid 24093205)
40. Stoylov SP, et al. 1997. Ordered aggregation of ribonucleic acids by the human immunodeficiency virus type 1 nucleocapsid protein. Biopolymers 41:301-312.
41. 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. (Pubitemid 38140599)
42. Vo MN, Barany G, Rouzina I, Musier-Forsyth K. 2009. HIV-1 nucleocapsid protein switches the pathway of transactivation response element RNA/DNA annealing from loop-loop "kissing" to "zipper." J. Mol. Biol. 386:789-801.
43. Vuilleumier C, et al. 1999. Nucleic acid sequence discrimination by the HIV-1 nucleocapsid protein NCp7: a fluorescence study. Biochemistry 38:16816-16825.
44. Vuilleumier C, Maechling-Strasser C, Gerard D, Mely Y. 1997. Evidence and prevention of HIV-1 nucleocapsid protein adsorption onto fluorescence quartz cells. Anal. Biochem. 244:183-185. (Pubitemid 27030548)
45. Williams MC, 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. (Pubitemid 32488203)
46. Ziegler A, Seelig J. 2004. Interaction of the protein transduction domain of HIV-1 TAT with heparan sulfate: binding mechanism and thermodynamic parameters. Biophys. J. 86:254-263. (Pubitemid 38067453)