Insights into the regioselectivity and RNA-binding affinity of HIV-1 nucleocapsid protein from linear-scaling quantum methods

Journal of Molecular Biology

Volumn 330, Issue 5, 2003, Pages 993-1004

  Khandogin, Jana ^a   Musier Forsyth, Karin ^a   York, Darrin M ^a  

^a University of Minnesota   (United States)

Author keywords

Chemical reactivity; Linear scaling quantum; Nucleocapsid protein; pKa; RNA binding

Indexed keywords

CYSTEINE; GENOMIC RNA; NUCLEOCAPSID PROTEIN;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; ELECTRIC ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS 1; LIFE CYCLE; LINEAR SYSTEM; MACROMOLECULE; MATHEMATICAL COMPUTING; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN RNA BINDING; PROTON TRANSPORT; RNA BINDING; ZINC FINGER MOTIF;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0038013705     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00658-2     Document Type: Article

References (78)

1. Tsuchihashi Z., Brown P.O. DNA strand exchange and selective DNA annealing promoted by the human immunodeficiency virus type 1 nucleocapsid protein. J. Virol. 68:1994;5863-5870.
2. 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.
3. Darlix J.-L., Lapadat-Tapolsky M., de Rocquigny H., Roques P.B. First glimpses at structure-function relationships of the nucleocapsid protein of retroviruses. J. Mol. Biol. 254:1995;523-537.
4. Herschlag D. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270:1995;20871-20874.
5. Lorsch J.R. RNA chaperones exist and DEAD box proteins get a life. Cell. 109:2002;797-801.
6. de Rocquigny H., Gabus C., Vincent A., Fournié-Zaluski M.-C., Roques B., Darlix J.-L. Viral RNA annealing activities of human immunodeficiency virus type 1 nucleocapsid protein require only peptide domains outside the zinc fingers. Proc. Natl Acad. Sci. USA. 89:1992;6472-6476.
7. Lys,3 with HIV-1 nucleocapsid protein. J. Mol. Biol. 306:2001;443-454.
8. Lys,3 structural changes but are not critical for primer/template annealing. J. Mol. Biol. 312:2001;985-997.
9. 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.
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. Rodríguez-Rodríguez 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.
12. 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.
13. Wu T., Guo J., Bess J., Henderson L.E., Levin J.G. Molecular requirements for human immunodeficiency virus type 1 plus-strand transfer: analysis in reconstituted and endogenous reverse transcription systems. J. Virol. 73:1999;4794-4805.
14. Lys,3 in the fidelity and efficacy of plus strand DNA transfer during HIV-1 reverse transcription. J. Biol. Chem. 274:1999;4412-4420.
15. Berg J.M. Potential metal-binding domains in nucleic acid binding proteins. Science. 232:1986;485-487.
16. 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.
17. Guo J., Wu T., Kane B.F., Johnson D.G., Henderson L.E., Gorelick R.J., Levin J.G. Subtle alterations of the native zinc finger structures have dramatic effects on the nucleic acid chaperone activity of human immunodeficiency virus type 1 nucleocapsid protein. J. Virol. 76:2002;4370-4378.
18. 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.
19. Williams M.C., Gorelick R.J., Musier-Forsyth K. Specific zinc-finger architecture required for HIV-1 nucleocapsid protein's nucleic acid chaperone function. Proc. Natl Acad. Sci. USA. 99:2002;8614-8619.
20. De Guzman R.N., Wu Z.R., Stalling C.C., Pappalardo L., Borer P.N., Summers M.F. Structure of the HIV-1 nucleocapsid protein bound to the SL3 Ψ-RNA recognition element. Science. 279:1998;384-388.
21. Amarasinghe G.K., De Guzman R.N., Turner R.B., Chancellor K.J., Wu Z.R., Summers M.F. NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the Ψ-RNA packaging signal. Implications for genome recognition. J. Mol. Biol. 301:2000;491-511.
22. Gorelick R.J., Nigida S.M. Jr, Bess J.W. Jr, Arthur L.O., Henderson L.E., Rein A. Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. J. Virol. 64:1990;3207-3211.
23. Gorelick R.J., Chabot D.J., Rein A., Henderson L.E., Arthur L.O. The two zinc fingers in the human immunodeficiency virus type 1 nucleocapsid protein are not functionally equivalent. J. Virol. 67:1993;4027-4036.
24. Gorelick R.J., Fu W., Gagliardi T.D., Bosche W.J., Rein A., Henderson L.E., Arthur L.O. Characterization of the block in replication of nucleocapsid protein zinc finger mutants from oloney murine leukemia virus. J. Virol. 73:1999;8185-8195.
25. 2+fingers are required for efficient reverse transcription, initial integration processes, and protection of newly synthesized viral DNA. J. Virol. 77:2003;1469-1480.
26. 23-Cys mutant nucleocapsid protein of HIV-1 indicate that the conformation of the first zinc finger is critical for virus infectivity. Biochemistry. 33:1994;11707-11716.
27. Tanchou V., Decimo D., Péchoux C., Lener D., Rogemond V., Berthoux L., Ottmann M., Darlix J.-L. Role of the N-terminal zinc finger of human immunodeficiency virus type 1 nucleocapsid protein in virus structure and replication. J. Virol. 72:1998;4442-4447.
28. Rice W.G., Schaeffer C.A., Harten B., Villinger F., South T.L., Summers M.F., et al. Inhibition of HIV-1 infectivity by zinc-ejecting aromatic C-nitroso compounds. Nature. 361:1993;473-475.
29. Tummino P.J., Scholten J.D., Harvey P.J., Holler T.P., Maloney L., Gogliotti R., et al. The in vitro ejection of zinc from human immunodeficiency virus (HIV) type 1 nucleocapsid protein by disulfide benzamides with cellular anti-HIV activity. Proc. Natl Acad. Sci. USA. 93:1996;969-973.
30. Huang M., Maynard A., Turpin J.A., Graham L., Janini G.M., Covell D.G., Rice W.G. Anti-HIV agents that selectively target retroviral nucleocapsid protein zinc fingers without affecting cellular zinc finger proteins. J. Med. Chem. 41:1998;1371-1381.
31. Turpin J.A., Song Y., Inman J.K., Huang M., Wallqvist A., Maynard A., et al. Synthesis and biological properties of novel pyridinioalkanoyl thiolesters (PATE) as anti-HIV-1 agents that target the viral nucleocapsid protein zinc fingers. J. Med. Chem. 42:1999;67-86.
32. Druillennec S., Dong C.Z., Escaich S., Gresh N., Bousseau A., Roques B.P., Fournié-Zaluski M.C. A mimic of HIV-1 nucleocapsid protein impairs reverse transcription and displays antiviral activity. Proc. Natl Acad. Sci. USA. 96:1999;4886-4891.
33. Stephen A.G., Worthy K.M., Towler E., Mikovits J.A., Sei S., Roberts P., et al. Identification of HIV-1 nucleocapsid protein:nucleic acid antagonists with cellular anti-HIV activity. Biochem. Biophys. Res. Commun. 296:2002;1228-1237.
34. Rice W.G., Schaeffer C.A., Graham L., Bu M., McDougal J.S., Orloff S.L., et al. The site of antiviral action of 3-nitrosobenzamide on the infectivity process of human immunodeficiency virus in human lymphocytes. Proc. Natl Acad. Sci. USA. 90:1993;9721-9724.
35. Rice W.G., Supko J.G., Malspeis L., Buckheit R.W. Jr, Clanton D., Bu M., et al. Inhibitors of HIV nucleocapsid protein zinc fingers as candidates for the treatment of aids. Science. 270:1995;1194-1197.
36. Rice W.G., Turpin J.A., Huang M., Clanton D., Buckheit R.W. Jr, Covell D.G., et al. Azodicarbonamide inhibits HIV-1 replication by targeting the nucleocapsid protein. Nature Med. 3:1997;341-345.
37. Hathout Y., Fabris D., Han M.S., Sowder R. II, Henderson L.E., Fenselau C. Characterization of intermediates in the oxidation of zinc fingers in human immunodeficiency virus type 1 nucleocapsid protein P7. Drug Metab. Dispos. 24:1997;1395-1400.
38. Chertova E.N., Kane B.P., McGrath C., Johnson D.G., Sowder R.C. II, Arthur L.O., Henderson L.E. Probing the topography of HIV-1 nucleocapsid protein with the alkylating agent N-ethylmaleimide. Biochemistry. 37:1998;17890-17897.
39. Basrur V., Song Y., Mazur S.J., Higashimoto Y., Turpin J.A., Rice W.G., et al. Inactivation of HIV-1 nucleocapsid protein p7 by pyridinioalkanoyl thioesters. Characterization of reaction products and proposed mechanism of action. J. Biol. Chem. 275:2000;14890-14897.
40. Topol I.A., Nemukhin A.V., Chao M., Iyer L.K., Tawa G.J., Burt S.K. Quantum chemical studies of reactions of the cyclic disulfides with the zinc finger domains in the HIV-1 nucleocapsid protein (NCp7). J. Am. Chem. Soc. 122:2000;7087-7094.
41. Topol I.A., Nemukhin A.V., Dobrogorskaya Y.I., Burt S.K. Interactions of azodicarbonamide (ADA) species with the model zinc finger site: theoretical support of the zinc finger domain destruction in the HIV-1 nucleocapsid protein (NCp7) by ADA. J. Phys. Chem. ser. B. 105:2001;11341-11350.
42. Maynard A.T., Huang M., Rice W.G., Covell D.G. Reactivity of the HIV-1 nucleocapsid protein p7 zinc finger domains from the perspective of density-functional theory. Proc. Natl Acad. Sci. USA. 95:1998;11578-11583.
43. Maynard A.T., Covell D.G. Reactivity of zinc finger cores: analysis of protein packing and electrostatic screening. J. Am. Chem. Soc. 123:2001;1047-1058.
44. York D.M., Lee T.-S., Yang W. Parameterization and efficient implementation of a solvent model for linear-scaling semiempirical quantum mechanical calculations of biological macromolecules. Chem. Phys. Letters. 263:1996;297-306.
45. York D.M., Karplus M. A smooth solvation potential based on the Conductor-Like Screening model. J. Phys. Chem. ser. A. 103:1999;11060-11079.
46. Goedecker S. Linear scaling electronic structure methods. Rev. Mod. Phys. 71:1999;1085-1123.
47. Honig B., Nicholls A. Classical electrostatics in biology and chemistry. Science. 268:1995;1144-1149.
48. Gilson M.K. Theory of electrostatic interactions in macromolecules. Curr. Opin. Struct. Biol. 5:1995;216-223.
49. Chin K., Sharp K.A., Honig B., Pyle A.M. Calculating the electrostatic properties of RNA provides new insights into molecular interactions and function. Nature Struct. Biol. 6:1999;1055-1061.
50. Pearson R.G. Chemical Hardness. 1997;Wiley-VCH, Weinheim.
51. Parr R., Yang W. Density-Functional Theory of Atoms and Molecules. 1989;Oxford University Press, New York.
52. Chermette H. Chemical reactivity indexes in density functional theory. J. Comput. Chem. 20:1999;129-154.
53. a's in proteins. Proteins: Struct. Funct. Genet. 15:1993;252-265.
54. a's in proteins. Biochemistry. 35:1996;7819-7833.
55. 2+. J. Mol. Biol. 310:2001;659-672.
56. 2+dissociation. Biochemistry. 41:2002;4312-4320.
57. Hendsch Z.S., Tidor B. Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci. 3:1994;211-226.
58. Xiao L., Honig B. Electrostatic contributions to the stability of hyperthermophilic proteins. J. Mol. Biol. 289:1999;1435-1444.
59. Kumar S., Nussinov R. Salt bridge stability in monomeric proteins. J. Mol. Biol. 293:1999;1241-1255.
60. Sheinerman F.B., Norel R., Honig B. Electrostatic aspects of protein protein interactions. Curr. Opin. Struct. Biol. 10:2000;153-159.
61. Norel R., Sheinerman F., Petrey D., Honig B. Electrostatic contributions to protein protein interactions: fast energetic filters for docking and their physical basis. Protein Sci. 10:2001;2147-2161.
62. Misra V.K., Honig B. On the magnitude of the electrostatic contribution to ligand-DNA interactions. Proc. Natl Acad. Sci. USA. 92:1995;4691-4695.
63. 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.
64. Mély Y., de Rocquigny H., Sorinas-Jimeno M., Keith G., Roques B.P., Marquet R. Binding of the HIV-1 nucleocapsid protein to the primer tRNA, in vitro, is essentially not specific. J. Biol. Chem. 270:1995;1650-1656.
65. Vuilleumier C., Bombarda E., Morellet N., Gérard D., Roques B.P., Mély Y. Nucleic acid sequence discrimination by the HIV-1 nucleocapsid protein NCp7: a fluorescence study. Biochemistry. 38:1999;16816-16825.
66. Urbaneja M.A., Kane B.P., Johnson D.G., Gorelick R.J., Henderson L.E., Casas-Finet J.R. Binding properties of the human immunodeficiency virus type 1 nucleocapsid protein p7 to a model RNA: elucidation of the structural determinants for function. J. Mol. Biol. 287:1999;59-75.
67. Berthoux L., Péchoux C., Ottmann M., Morel G., Darlix J.-L. Mutations in the N-terminal domain of human immunodeficiency virus type 1 nucleocapsid protein affect virion core structure and proviral DNA synthesis. J. Virol. 71:1997;6973-6981.
68. Dannull J., Surovoy A., Jung G., Moelling K. Specific binding of HIV-1 nucleocapsid protein to Ψ RNA in vitro requires N-terminal zinc finger and flanking basic amino acid residues. EMBO J. 13:1994;1525-1533.
69. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., Karplus M. Charmm: a program for macromolecular energy minimization and dynamics calculations. J. Comput. Chem. 4:1983;187-217.
70. MacKerell A.D. Jr, Brooks B., Brooks C.L. III, Nilsson L., Roux B., Won Y., Karplus M. CHARMM: the energy function and its parameterization with an overview of the program. Schleyer P., Allinger N., Clark T., Gasteiger J., Kollman P., Schaefer H. III, Schreiner P. Encyclopedia of Computational Chemistry. vol. 1:1998;271-277 Wiley, Chichester.
71. MacKerell A.D. Jr, Bashford D., Bellott M., Dunbrack R.L. Jr, Evanseck J.D., Field M.J., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. ser. B. 102:1998;3586-3616.
72. Foloppe N., MacKerell A.D. Jr. All-atom empirical force field for nucleic acids: I. Parameter optimization based on small molecule and condensed phase macromolecular target data. J. Comput. Chem. 21:2000;86-104.
73. Stote R.H., Karplus M. Zinc binding in proteins and solution: a simple but accurate nonbonded representation. Proteins: Struct. Funct. Genet. 23:1995;12-31.
74. Klamt A., Schüürmann G. COSMO: a new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient. J. Chem. Soc., Perkin Trans. 2. 2:1993;799-805.
75. Lewis J.P., Liu S., Lee T.-S., Yang W. A linear-scaling quantum mechanical investigation of cytidine deaminase. J. Comput. Phys. 151:1999;242-263.
76. Li J., Zhu T., Cramer C.J., Truhlar D.G. New class IV charge model for extracting accurate partial charges from wave functions. J. Phys. Chem. ser. A. 102:1998;1820-1831.
77. Nicholls A., Sharp K.A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
78. Stewart J.J.P. Optimization of parameters for semiempirical methods. I. Method. J. Comput. Chem. 10:1989;209-220.