Impact of the terminal bulges of HIV-1 cTAR DNA on its stability and the destabilizing activity of the nucleocapsid protein NCp7

Journal of Molecular Biology

Volumn 328, Issue 1, 2003, Pages 95-108

  Beltz, Hervé ^a   Azoulay, Joel ^a   Bernacchi, Serena ^a   Clamme, Jean Pierre ^a   Ficheux, Damien ^b   Roques, Bernard ^c   Darlix, Jean Luc ^d   Mély, Yves ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^c Laboratoire de Pharmacochimie   (France)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

Bulge; Fluorescence correlation spectroscopy; NCp7; TAR; Time resolved fluorescence

Indexed keywords

ADENINE; COMPLEMENTARY DNA; CYTOSINE; DNA BASE; GUANINE; NUCLEOCAPSID PROTEIN; PROTEIN NCP7; RNA; UNCLASSIFIED DRUG;

ARTICLE; BASE MISPAIRING; BASE PAIRING; CHEMICAL LABELING; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; DNA SEQUENCE; ENERGY; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MUTANT; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PHOTON; PRIORITY JOURNAL; PROTEIN STABILITY; THERMODYNAMICS; TRANSACTIVATION; VIRUS STRAIN;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0037453234     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00244-4     Document Type: Article

References (76)

1. Arts E.J., Wainberg M.A. Human immunodeficiency virus type 1 reverse transcriptase and early events in reverse transcription. Advan. Virus Res. 46:1996;97-163.
2. Guo J., Henderson L.E., Bess J., Kane B., Levin J.G. 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. 71:1997;5178-5188.
3. Lapadat-Tapolsky M., Gabus C., Rau M., Darlix J.L. Possible roles of HIV-1 nucleocapsid protein in the specificity of proviral DNA synthesis and in its variability. J. Mol. Biol. 268:1997;250-260.
4. Lapadat-Tapolsky M., Pernelle C., Borie C., Darlix J.L. Analysis of the nucleic acid annealing activities of nucleocapsid protein from HIV-1. Nucl. Acids Res. 23:1995;2434-2441.
5. Baudin F., Marquet R., Isel C., Darlix J.L., Ehresmann B., Ehresmann C. Functional sites in the 5′ region of human immunodeficiency virus type 1 RNA form defined structural domains. J. Mol. Biol. 229:1993;382-397.
6. You J.C., McHenry C.S. HIV nucleocapsid protein. Expression in Escherichia coli, purification, and characterization. J. Biol. Chem. 268:1993;16519-16527.
7. Jeeninga R.E., Huthoff H.T., Gultyaev A.P., Berkhout B. The mechanism of actinomycin D-mediated inhibition of HIV-1 reverse transcription. Nucl. Acids Res. 26:1998;5472-5479.
8. Driscoll M.D., Hughes S.H. Human immunodeficiency virus type 1 nucleocapsid protein can prevent self-priming of minus-strand strong stop DNA by promoting the annealing of short oligonucleotides to hairpin sequences. J. Virol. 74:2000;8785-8792.
9. Rodriguez-Rodriguez L., Tsuchihashi Z., Fuentes G.M., Bambara R.A., Fay P.J. Influence of human immunodeficiency virus nucleocapsid protein on synthesis and strand transfer by the reverse transcriptase in vitro. J. Biol. Chem. 270:1995;15005-15011.
10. You J.C., McHenry C.S. Human immunodeficiency virus nucleocapsid protein accelerates strand transfer of the terminally redundant sequences involved in reverse transcription. J. Biol. Chem. 269:1994;31491-31495.
11. Peliska J.A., Balasubramanian S., Giedroc D.P., Benkovic S.J. Recombinant HIV-1 nucleocapsid protein accelerates HIV-1 reverse transcriptase catalyzed DNA strand transfer reactions and modulates RNase H activity. Biochemistry. 33:1994;13817-13823.
12. Kim J.K., Palaniappan C., Wu W., Fay P.J., Bambara R.A. Evidence for a unique mechanism of strand transfer from the transactivation response region of HIV-1. J. Biol. Chem. 272:1997;16769-16777.
13. Guo J., Wu T., Anderson J., Kane B.F., Johnson D.G., Gorelick R.J., et al. Zinc finger structures in the human immunodeficiency virus type 1 nucleocapsid protein facilitate efficient minus- and plus-strand transfer. J. Virol. 74:2000;8980-8988.
14. DeStefano J.J. Human immunodeficiency virus nucleocapsid protein stimulates strand transfer from internal regions of heteropolymeric RNA templates. Arch. Virol. 140:1995;1775-1789.
15. Davis W.R., Gabbara S., Hupe D., Peliska J.A. Actinomycin D inhibition of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase and nucleocapsid protein. Biochemistry. 37:1998;14213-14221.
16. Darlix J.L., Vincent A., Gabus C., de Rocquigny H., Roques B. Trans-activation of the 5′ to 3′ viral DNA strand transfer by nucleocapsid protein during reverse transcription of HIV1 RNA. C R Acad. Sci. III. 316:1993;763-771.
17. Allain B., Lapadat-Tapolsky M., Berlioz C., Darlix J.L. Transactivation of the minus-strand DNA transfer by nucleocapsid protein during reverse transcription of the retroviral genome. EMBO J. 13:1994;973-981.
18. Henderson L.E., Bowers M.A., Sowder R.C. 2nd, Serabyn S.A., Johnson D.G., Bess J.W. Jr, et al. Gag proteins of the highly replicative MN strain of human immunodeficiency virus type 1: posttranslational modifications, proteolytic processings, and complete amino acid sequences. J. Virol. 66:1992;1856-1865.
19. Cimarelli A., Darlix J.L. Assembling the human immunodeficiency virus type 1. Cell Mol. Life Sci. 59:2002;1166-1184.
20. Coffin J.M. Structure of the Retroviral Genome. 1984;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
21. Darlix J.L., Lapadat-Tapolsky M., de Rocquigny H., Roques B.P. First glimpses at structure-function relationships of the nucleocapsid protein of retroviruses. J. Mol. Biol. 254:1995;523-537.
22. Guo J., Wu T., Bess J., Henderson L.E., Levin J.G. Actinomycin D inhibits human immunodeficiency virus type 1 minus-strand transfer in in vitro and endogenous reverse transcriptase assays. J. Virol. 72:1998;6716-6724.
23. Rein A., Henderson L.E., Levin J.G. Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem. Sci. 23:1998;297-301.
24. Cristofari G., Darlix J.L. The ubiquitous nature of RNA chaperone proteins. Prog. Nucl. Acid Res. Mol. Biol. 72:2002;223-268.
25. Hargittai M.R., Mangla A.T., Gorelick R.J., Musier-Forsyth K. HIV-1 nucleocapsid protein zinc finger structures induce tRNA(Lys,3) structural changes but are not critical for primer/template annealing. J. Mol. Biol. 312:2001;985-997.
26. Williams M.C., Rouzina I., Wenner J.R., Gorelick R.J., Musier-Forsyth K., Bloomfield V.A. Mechanism for nucleic acid chaperone activity of HIV-1 nucleocapsid protein revealed by single molecule stretching. Proc. Natl Acad. Sci. USA. 98:2001;6121-6126.
27. Johnson P.E., Turner R.B., Wu Z.R., Hairston L., Guo J., Levin J.G., Summers M.F. A mechanism for plus-strand transfer enhancement by the HIV-1 nucleocapsid protein during reverse transcription. Biochemistry. 39:2000;9084-9091.
28. Bernacchi S., Stoylov S., Piemont E., Ficheux D., Roques B.P., Darlix J.L., Mely Y. HIV-1 nucleocapsid protein activates transient melting of least stable parts of the secondary structure of TAR and its complementary sequence. J. Mol. Biol. 317:2002;385-399.
29. Azoulay J., Clamme J.P., Darlix J.L., Roques B.P., Mély Y. Destabilization of the HIV-1 complementary sequence of TAR by the nucleocapsid protein through activation of conformational fluctuations. J. Mol. Biol. 362:2003;691-700.
30. Hong M.K., Harbron E.J., O'Connor D.B., Guo J., Barbara P.F., Levin J.G., Musier-Forsyth K. Nucleic acid conformational changes essential for HIV-1 nucleocapsid protein-mediated inhibition of self-priming in minus-strand transfer. J. Mol. Biol. 325:2003;1-10.
31. Vallone P.M., Paner T.M., Hilario J., Lane M.J., Faldasz B.D., Benight A.S. Melting studies of short DNA hairpins: influence of loop sequence and adjoining base pair identity on hairpin thermodynamic stability. Biopolymers. 50:1999;425-442.
32. LeBlanc D.A., Morden K.M. Thermodynamic characterization of deoxyribooligonucleotide duplexes containing bulges. Biochemistry. 30:1991;4042-4047.
33. Bloomfield V.A., Crothers D.M., Tinoco I. Jr. Nucleic Acids Structures, Properties, and Functions. 2000;University Science Books, Sausalito, CA.
34. Cantor C.R., Schimmel P.R. Biophysical Chemistry. 1980;Freeman W. H. San Francisco, CA.
35. Hilbers C.W., Haasnoot C.A., de Bruin S.H., Joordens J.J., van der Marel G.A., van Boom J.H. Hairpin formation in synthetic oligonucleotides. Biochimie. 67:1985;685-695.
36. Berkhout B., Vastenhouw N.L., Klasens B.I., Huthoff H. Structural features in the HIV-1 repeat region facilitate strand transfer during reverse transcription. RNA. 7:2001;1097-1114.
37. Bernacchi S., Mely Y. Exciton interaction in molecular beacons: a sensitive sensor for short range modifications of the nucleic acid structure. Nucl. Acids Res. 29:2001;E62-2.
38. Bernacchi S., Piemont E., Potier N., Dorsselaer A., Mely Y. Excitonic heterodimer formation in an HIV-1 oligonucleotide labeled with a donor-acceptor pair used for fluorescence resonance energy transfer. Biophys. J. 84:2003;643-654.
39. Stoylov S.P., Vuilleumier C., Stoylova E., De Rocquigny H., Roques B.P., Gerard D., Mely Y. Ordered aggregation of ribonucleic acids by the human immunodeficiency virus type 1 nucleocapsid protein. Biopolymers. 41:1997;301-312.
40. Fisher R.J., Rein A., Fivash M., Urbaneja M.A., Casas-Finet J.R., Medaglia M., Henderson L.E. Sequence-specific binding of human immunodeficiency virus type 1 nucleocapsid protein to short oligonucleotides. J. Virol. 72:1998;1902-1909.
41. Vuilleumier C., Bombarda E., Morellet N., Gerard D., Roques B.P., Mely Y. Nucleic acid sequence discrimination by the HIV-1 nucleocapsid protein NCp7: a fluorescence study. Biochemistry. 38:1999;16816-16825.
42. Hess S.T., Huang S., Heikal A.A., Webb W.W. Biological and chemical applications of fluorescence correlation spectroscopy: a review. Biochemistry. 41:2002;697-705.
43. Krichevsky O., Bonnet G. Fluorescence correlation spectroscopy: the technique and its applications. Rep. Prog. Phys. 65:2002;251-297.
44. Bonnet G., Krichevsky O., Libchaber A. Kinetics of conformational fluctuations in DNA hairpin-loops. Proc. Natl Acad. Sci. USA. 95:1998;8602-8606.
45. Antao V.P., Tinoco I. Jr. Thermodynamic parameters for loop formation in RNA and DNA hairpin tetraloops. Nucl. Acids Res. 20:1992;819-824.
46. Senior M.M., Jones R.A., Breslauer K.J. Influence of loop residues on the relative stabilities of DNA hairpin structures. Proc. Natl Acad. Sci. USA. 85:1988;6242-6246.
47. Blommers M.J., Walters J.A., Haasnoot C.A., Aelen J.M., van der Marel G.A., van Boom J.H., Hilbers C.W. Effects of base sequence on the loop folding in DNA hairpins. Biochemistry. 28:1989;7491-7498.
48. Groebe D.R., Uhlenbeck O.C. Thermal stability of RNA hairpins containing a four-membered loop and a bulge nucleotide. Biochemistry. 28:1989;742-747.
49. Znosko B.M., Silvestri S.B., Volkman H., Boswell B., Serra M.J. Thermodynamic parameters for an expanded nearest-neighbor model for the formation of RNA duplexes with single nucleotide bulges. Biochemistry. 41:2002;10406-10417.
50. Longfellow C.E., Kierzek R., Turner D.H. Thermodynamic and spectroscopic study of bulge loops in oligoribonucleotides. Biochemistry. 29:1990;278-285.
51. Mathews D.H., Sabina J., Zuker M., Turner D.H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288:1999;911-940.
52. Woodson S.A., Crothers D.M. Proton nuclear magnetic resonance studies on bulge-containing DNA oligonucleotides from a mutational hot-spot sequence. Biochemistry. 26:1987;904-912.
53. SantaLucia J. Jr. A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc. Natl Acad. Sci. USA. 95:1998;1460-1465.
54. Allawi H.T., SantaLucia J. Jr. Thermodynamics and NMR of internal G·T mismatches in DNA. Biochemistry. 36:1997;10581-10594.
55. Rouzina I., Bloomfield V.A. Heat capacity effects on the melting of DNA. 2. Analysis of nearest-neighbor base pair effects. Biophys. J. 77:1999;3252-3255.
56. Rouzina I., Bloomfield V.A. Heat capacity effects on the melting of DNA. 1. General aspects. Biophys. J. 77:1999;3242-3251.
57. Cain R.J., Glick G.D. The effect of cross-links on the conformational dynamics of duplex DNA. Nucl. Acids Res. 25:1997;836-842.
58. Nonin S., Leroy J.L., Gueron M. Terminal base pairs of oligodeoxynucleotides: imino proton exchange and fraying. Biochemistry. 34:1995;10652-10659.
59. Leroy J.L., Charretier E., Kochoyan M., Gueron M. Evidence from base-pair kinetics for two types of adenine tract structures in solution: their relation to DNA curvature. Biochemistry. 27:1988;8894-8898.
60. Takahashi K.I., Baba S., Chattopadhyay P., Koyanagi Y., Yamamoto N., Takaku H., Kawai G. Structural requirement for the two-step dimerization of human immunodeficiency virus type 1 genome. RNA. 6:2000;96-102.
61. Clever J., Sassetti C., Parslow T.G. RNA secondary structure and binding sites for gag gene products in the 5′ packaging signal of human immunodeficiency virus type 1. J. Virol. 69:1995;2101-2109.
62. Damgaard C.K., Dyhr-Mikkelsen H., Kjems J. 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. 26:1998;3667-3676.
63. Sykora K.W., Moelling K. Properties of the avian viral protein p12. J. Gen. Virol. 55:1981;379-391.
64. Urbaneja M.A., Wu M., Casas-Finet J.R., Karpel R.L. HIV-1 nucleocapsid protein as a nucleic acid chaperone: spectroscopic study of its helix-destabilizing properties, structural binding specificity, and annealing activity. J. Mol. Biol. 318:2002;749-764.
65. Tisne C., Roques B.P., Dardel F. Heteronuclear NMR studies of the interaction of tRNA(Lys)3 with HIV-1 nucleocapsid protein. J. Mol. Biol. 306:2001;443-454.
66. Mely Y., de Rocquigny H., Sorinas-Jimeno M., Keith G., Roques B.P., Marquet R., Gerard D. Binding of the HIV-1 nucleocapsid protein to the primer tRNA(3Lys), in vitro, is essentially not specific. J. Biol. Chem. 270:1995;1650-1656.
67. Clever J.L., Eckstein D.A., Parslow T.G. Genetic dissociation of the encapsidation and reverse transcription functions in the 5′ R region of human immunodeficiency virus type 1. J. Virol. 73:1999;101-109.
68. Harrich D., Ulich C., Gaynor R.B. A critical role for the TAR element in promoting efficient human immunodeficiency virus type 1 reverse transcription. J. Virol. 70:1996;4017-4027.
69. Harrich D., Hooker C.W., Parry E. The human immunodeficiency virus type 1 TAR RNA upper stem-loop plays distinct roles in reverse transcription and RNA packaging. J. Virol. 74:2000;5639-5646.
70. Berkhout B., Klaver B., Das A.T. Forced evolution of a regulatory RNA helix in the HIV-1 genome. Nucl. Acids Res. 25:1997;940-947.
71. Klaver B., Berkhout B. Evolution of a disrupted TAR RNA hairpin structure in the HIV-1 virus. EMBO J. 13:1994;2650-2659.
72. Williams M.C., Rouzina I., Bloomfield V.A. Thermodynamics of DNA interactions from single molecule stretching experiments. Acc. Chem. Res. 35:2002;159-166.
73. De Rocquigny H., Ficheux D., Gabus C., Fournie-Zaluski M.C., Darlix J.L., Roques B.P. First large scale chemical synthesis of the 72 amino acid HIV-1 nucleocapsid protein NCp7 in an active form. Biochem. Biophys. Res. Commun. 180:1991;1010-1018.
74. Livesey A.K., Brochon J.C. Analyzing the distribution of decay constants in pulse-fluorimetry using the maximum entropy method. Biophys. J. 52:1987;693-706.
75. Clamme J.P., Azoulay J., Mély Y. Monitoring of the formation and dissociation of polyethylenimine/DNA complexes by two photon fluorescence correlation spectroscopy. Biophys. J. 84:2003;1960-1968.
76. Thompson N.L. Lakowicz J.R. Topics in Fluorescence Spectroscopy. vol. 1:1991;337-410 Plenum Press, New York.