Intrinsic nucleic acid dynamics modulates HIV-1 nucleocapsid protein binding to its targets

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Bazzi, Ali ^a   Zargarian, Loussiné ^a   Chaminade, Françoise ^a   de Rocquigny, Hugues ^b   René, Brigitte ^a   Mély, Yves ^b   Fossé, Philippe ^a   Mauffret, Olivier ^a  

^a CNRS   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE; NUCLEIC ACID; NUCLEOCAPSID PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BASE PAIRING; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE; PROTEIN BINDING;

DNA, VIRAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HIV-1; MAGNETIC RESONANCE SPECTROSCOPY; NUCLEIC ACID CONFORMATION; NUCLEOCAPSID PROTEINS; PROTEIN BINDING;

EID: 84862688471     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038905     Document Type: Article

References (68)

1. Darlix JL, Godet J, Ivanyi-Nagy R, Fosse P, Mauffret O, et al. (2011) Flexible nature and specific functions of the HIV-1 nucleocapsid protein. J Mol Biol 410: 565-581.
2. 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.
3. Thomas JA, Gorelick RJ, (2008) Nucleocapsid protein function in early infection processes. Virus Research 134: 39-63.
4. Darlix JL, Garrido JL, Morellet N, Mely Y, de Rocquigny H, (2007) Properties, functions, and drug targeting of the multifunctional nucleocapsid protein of the human immunodeficiency virus. Adv Pharmacol 55: 299-346.
5. Godet J, Mely Y, (2010) Biophysical studies of the nucleic acid chaperone properties of the HIV-1 nucleocapsid protein. RNA Biol 7: 48-60.
6. Levin JG, Mitra M, Mascarenhas A, Musier-Forsyth K, (2010) Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription. RNA Biol 7.
7. Mirambeau G, Lyonnais S, Gorelick RJ, (2010) Features, processing states, and heterologous protein interactions in the modulation of the retroviral nucleocapsid protein function. RNA Biol 7: 85-95.
8. Muriaux D, Darlix JL, (2010) Properties and functions of the nucleocapsid protein in virus assembly. RNA Biol 7.
9. Amarasinghe GK, De Guzman RN, Turner RB, Summers MF, (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.
10. Vuilleumier C, Bombarda E, Morellet N, Gerard D, Roques BP, et al. (1999) Nucleic acid sequence discrimination by the HIV-1 nucleocapsid protein NCp7: a fluorescence study. Biochemistry 38: 16816-16825.
11. 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.
12. Lapadat-Tapolsky M, De Rocquigny H, Van Gent D, Roques B, Plasterk R, et al. (1993) Interactions between HIV-1 nucleocapsid protein and viral DNA may have important functions in the viral life cycle. Nucleic Acids Res 21: 831-839.
13. Beltz H, Clauss C, Piemont E, Ficheux D, Gorelick RJ, 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.
14. Kanevsky I, Chaminade F, Ficheux D, Moumen A, Gorelick R, et al. (2005) Specific interactions between HIV-1 nucleocapsid protein and the TAR element. J Mol Biol 348: 1059-1077.
15. Kanevsky I, Chaminade F, Chen Y, Godet J, Rene B, et al. (2011) Structural determinants of TAR RNA-DNA annealing in the absence and presence of HIV-1 nucleocapsid protein. Nucleic Acids Res 39: 8148-8162.
16. Wang H, Yeh YS, Barbara PF, (2009) HIV-1 nucleocapsid protein bends double-stranded nucleic acids. J Am Chem Soc 131: 15534-15543.
17. 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.
18. Fisher RJ, Rein A, Fivash M, Urbaneja MA, Casas-Finet JR, et al. (1998) Sequence-specific binding of human immunodeficiency virus type 1 nucleocapsid protein to short oligonucleotides. J Virol 72: 1902-1909.
19. Bourbigot S, Ramalanjaona N, Boudier C, Salgado GF, Roques BP, 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.
20. Bazzi A, Zargarian L, Chaminade F, Boudier C, De Rocquigny H, et al. (2011) Structural insights into the cTAR DNA recognition by the HIV-1 nucleocapsid protein: role of sugar deoxyriboses in the binding polarity of NC. Nucleic Acids Res.
21. Morellet N, Demene H, Teilleux V, Huynh-Dinh T, de Rocquigny H, et al. (1998) Structure of the complex between the HIV-1 nucleocapsid protein NCp7 and the single-stranded pentanucleotide d(ACGCC). J Mol Biol 283: 419-434.
22. Lu K, Heng X, Summers MF, (2011) Structural Determinants and Mechanism of HIV-1 Genome Packaging. J Mol Biol 410: 609-633.
23. Watts JM, Dang KK, Gorelick RJ, Leonard CW, Bess JW Jr, et al. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460: 711-716.
24. Gherghe C, Lombo T, Leonard CW, Datta SA, Bess JW Jr, et al. (2010) Definition of a high-affinity Gag recognition structure mediating packaging of a retroviral RNA genome. Proc Natl Acad Sci U S A 107: 19248-19253.
25. Zargarian L, Kanevsky I, Bazzi A, Boynard J, Chaminade F, et al. (2009) Structural and dynamic characterization of the upper part of the HIV-1 cTAR DNA hairpin. Nucleic Acids Res 37: 4043-4054.
26. Godet J, de Rocquigny H, Raja C, Glasser N, Ficheux D, 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.
27. Vo MN, Barany G, Rouzina I, Musier-Forsyth K, (2006) Mechanistic studies of mini-TAR RNA/DNA annealing in the absence and presence of HIV-1 nucleocapsid protein. J Mol Biol 363: 244-261.
28. Vo MN, Barany G, Rouzina I, Musier-Forsyth K, (2009) Effect of Mg(2+) and Na(+) on the nucleic acid chaperone activity of HIV-1 nucleocapsid protein: implications for reverse transcription. J Mol Biol 386: 773-788.
29. Basu VP, Song M, Gao L, Rigby ST, Hanson MN, et al. (2008) Strand transfer events during HIV-1 reverse transcription. Virus Res 134: 19-38.
30. Al-Hashimi HM, Gosser Y, Gorin A, Hu W, Majumdar A, et al. (2002) Concerted motions in HIV-1 TAR RNA may allow access to bound state conformations: RNA dynamics from NMR residual dipolar couplings. J Mol Biol 315: 95-102.
31. Aboulela F, Karn J, Varani G, (1995) The Structure of the Human-Immunodeficiency-Virus Type-1 Tar Rna Reveals Principles of Rna Recognition by Tat Protein. J Mol Biol 253: 313-332.
32. Puglisi JD, Tan RY, Calnan BJ, Frankel AD, Williamson JR, (1992) Conformation of the Tar Rna-Arginine Complex by Nmr-Spectroscopy. Science 257: 76-80.
33. Zhang Q, Sun X, Watt ED, Al-Hashimi HM, (2006) Resolving the motional modes that code for RNA adaptation. Science 311: 653-656.
34. Zhang Q, Stelzer AC, Fisher CK, Al-Hashimi HM, (2007) Visualizing spatially correlated dynamics that directs RNA conformational transitions. Nature 450: 1263-1267.
35. Bothe JR, Nikolova EN, Eichhorn CD, Chugh J, Hansen AL, et al. (2011) Characterizing RNA dynamics at atomic resolution using solution-state NMR spectroscopy. Nat Methods 8: 919-931.
36. Mittermaier A, Kay LE, (2006) New tools provide new insights in NMR studies of protein dynamics. Science 312: 224-228.
37. Mittermaier AK, Kay LE, (2009) Observing biological dynamics at atomic resolution using NMR. Trends Biochem Sci 34: 601-611.
38. Palmer AG, 3rd, Kroenke CD, Loria JP (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol 339: 204-238.
39. Palmer AG 3rd, Massi F (2006) Characterization of the dynamics of biomacromolecules using rotating-frame spin relaxation NMR spectroscopy. Chem Rev 106: 1700-1719.
40. Shvadchak VV, Klymchenko AS, de Rocquigny H, Mely Y, (2009) Sensing peptide-oligonucleotide interactions by a two-color fluorescence label: application to the HIV-1 nucleocapsid protein. Nucleic Acids Res 37: e25.
41. Boisbouvier J, Wu Z, Ono A, Kainosho M, Bax A, (2003) Rotational diffusion tensor of nucleic acids from 13C NMR relaxation. J Biomol NMR 27: 133-142.
42. Duchardt E, Schwalbe H, (2005) Residue specific ribose and nucleobase dynamics of the cUUCGg RNA tetraloop motif by MNMR 13C relaxation. J Biomol NMR 32: 295-308.
43. Ying JF, Grishaev A, Bryce DL, Bax A, (2006) Chemical shift tensors of protonated base carbons in helical RNA and DNA from NMR relaxation and liquid crystal measurements. Journal of the American Chemical Society 128: 11443-11454.
44. Shajani Z, Varani G, (2008) 13C relaxation studies of the DNA target sequence for hhai methyltransferase reveal unique motional properties. Biochemistry 47: 7617-7625.
45. Bryce DL, Grishaev A, Bax A, (2005) Measurement of ribose carbon chemical shift tensors for A-form RNA by liquid crystal NMR spectroscopy. Journal of the American Chemical Society 127: 7387-7396.
46. Mandel AM, Akke M, Palmer AG, 3rd (1995) Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J Mol Biol 246: 144-163.
47. Shajani Z, Varani G, (2005) 13C NMR relaxation studies of RNA base and ribose nuclei reveal a complex pattern of motions in the RNA binding site for human U1A protein. J Mol Biol 349: 699-715.
48. Yamazaki T, Muhandiram R, Kay LE, (1994) Nmr Experiments for the Measurement of Carbon Relaxation Properties in Highly Enriched, Uniformly C-13,N-15-Labeled Proteins- Application to C-13(Alpha) Carbons. Journal of the American Chemical Society 116: 8266-8278.
49. Bryce DL, Grishaev A, Bax A, (2005) Measurement of ribose carbon chemical shift tensors for A-form RNA by liquid crystal NMR spectroscopy. J Am Chem Soc 127: 7387-7396.
50. Ying J, Grishaev A, Bryce DL, Bax A, (2006) Chemical shift tensors of protonated base carbons in helical RNA and DNA from NMR relaxation and liquid crystal measurements. J Am Chem Soc 128: 11443-11454.
51. Oberstrass FC, Allain FH, Ravindranathan S, (2008) Changes in dynamics of SRE-RNA on binding to the VTS1p-SAM domain studied by 13C NMR relaxation. J Am Chem Soc 130: 12007-12020.
52. Dethoff EA, Hansen AL, Musselman C, Watt ED, Andricioaei I, et al. (2008) Characterizing complex dynamics in the transactivation response element apical loop and motional correlations with the bulge by NMR, molecular dynamics, and mutagenesis. Biophys J 95: 3906-3915.
53. Tjandra N, Feller SE, Pastor RW, Bax A, (1995) Rotational diffusion anisotropy of human ubiquitin from N-15 NMR relaxation. Journal of the American Chemical Society 117: 12562-12566.
54. Hansen AL, Al-Hashimi HM, (2007) Dynamics of large elongated RNA by NMR carbon relaxation. J Am Chem Soc 129: 16072-16082.
55. Rule GS, Hitchens TK, (2006) Fundamentals of Protein NMR Spectroscopy. Netherlands: Springer.
56. Palmer RF, Blanchard S, Jean CR, Mandell DS, (2005) School district resources and identification of children with autistic disorder. Am J Public Health 95: 125-130.
57. Beltz H, Azoulay J, Bernacchi S, Clamme JP, Ficheux D, 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.
58. 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.
59. Spriggs S, Garyu L, Connor R, Summers MF, (2008) Potential intra- and intermolecular interactions involving the unique-5′ region of the HIV-1 5′-UTR. Biochemistry 47: 13064-13073.
60. Amarasinghe GK, De Guzman RN, Turner RB, Chancellor KJ, Wu ZR, 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.
61. Schroeder SJ, Turner DH, (2000) Factors affecting the thermodynamic stability of small asymmetric internal loops in RNA. Biochemistry 39: 9257-9274.
62. Sun X, Zhang Q, Al-Hashimi HM, (2007) Resolving fast and slow motions in the internal loop containing stem-loop 1 of HIV-1 that are modulated by Mg2+ binding: role in the kissing-duplex structural transition. Nucleic Acids Res 35: 1698-1713.
63. Olsen GL, Echodu DC, Shajani Z, Bardaro MF, Varani G, et al. (2008) Solid-state deuterium NMR studies reveal mu s-ns motions in the HIV-1 Transactivation response RNA recognition site. Journal of the American Chemical Society 130: 2896-2897.
64. Olsen GL, Bardaro MF, Echodu DC, Drobny GP, Varani G, (2010) Intermediate Rate Atomic Trajectories of RNA by Solid-State NMR Spectroscopy. Journal of the American Chemical Society 132: 303-308.
65. Pappalardo L, Kerwood DJ, Pelczer I, Borer PN, (1998) Three-dimensional folding of an RNA hairpin required for packaging HIV-1. J Mol Biol 282: 801-818.
66. Mely Y, Piemont E, Sorinas-Jimeno M, de Rocquigny H, Jullian N, et al. (1993) Structural and dynamic characterization of the aromatic amino acids of the human immunodeficiency virus type I nucleocapsid protein zinc fingers and their involvement in heterologous tRNA(Phe) binding: a steady-state and time-resolved fluorescence study. Biophys J 65: 1513-1522.
67. 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.
68. Godet J, Ramalanjaona N, Sharma KK, Richert L, de Rocquigny H, 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.