Comparative structural effects of HIV-1 gag and nucleocapsid proteins in binding to and unwinding of the viral RNA packaging signal

Biochemistry

Volumn 51, Issue 15, 2012, Pages 3162-3169

  Bell, Neil M ^a   Kenyon, Julia C ^a   Balasubramanian, Shankar ^a,b   Lever, Andrew M L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2-AMINOPURINE; CHAPERONE ACTIVITY; CHAPERONE FUNCTIONS; DISSOCIATION CONSTANT; FLUORESCENCE POLARIZATION; FLUORESCENCE PROPERTIES; GENOMIC RNA; LOOP STRUCTURE; NUCLEOCAPSID DOMAINS; NUCLEOCAPSID PROTEINS; RNA BINDING; RNA STRUCTURES; SPECIFIC CAPTURE; STEM-LOOP; STRUCTURAL EFFECT; VIRAL PROTEINS; VIRAL RNA;

DISSOCIATION; FLUORESCENCE; GENES; PROTEINS;

RNA;

2 AMINOPURINE; CHAPERONE; GAG PROTEIN; NUCLEIC ACID; NUCLEOCAPSID PROTEIN; VIRUS RNA;

ARTICLE; DISSOCIATION CONSTANT; FLUORESCENCE POLARIZATION; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR BEACON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RNA BINDING; RNA STRUCTURE; STRUCTURE ANALYSIS; VIRUS CAPSID; VIRUS GENOME;

2-AMINOPURINE; BINDING SITES; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; KINETICS; NUCLEIC ACID CONFORMATION; NUCLEOCAPSID PROTEINS; RNA, VIRAL; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84859927906     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2017969     Document Type: Article

References (49)

1. Gheysen, D., Jacobs, E., Deforesta, F., Thiriart, C., Francotte, M., Thines, D., and Dewilde, M. (1989) Assembly and Release of HIV-1 Precursor Pr55Gag Virus-Like Particles from Recombinant Baculovirus-Infected Insect Cells Cell 59, 103-112 (Pubitemid 19248562)
2. Lever, A. M. (2007) HIV-1 RNA packaging Adv. Pharmacol. 55, 1-32
3. Rein, A., Datta, S. A., Jones, C. P., and Musier-Forsyth, K. (2011) Diverse interactions of retroviral Gag proteins with RNAs Trends Biochem. Sci. 36, 373-380
4. Zeffman, A., Hassard, S., Varani, G., and Lever, A. (2000) The major HIV-1 packaging signal is an extended bulged stem loop whose structure is altered on interaction with the gag polyprotein J. Mol. Biol. 297, 877-893
5. Wu, T. Y., Datta, S. A. K., Mitra, M., Gorelick, R. J., Rein, A., and Levin, J. G. (2010) Fundamental differences between the nucleic acid chaperone activities of HIV-1 nucleocapsid protein and Gag or Gag-derived proteins: Biological implications Virology 405, 556-567
6. Cruceanu, M., Urbaneja, M. A., Hixson, C. V., Johnson, D. G., Datta, S. A., Fivash, M. J., Stephen, A. G., Fisher, R. J., Gorelick, R. J., Casas-Finet, J. R., Rein, A., Rouzina, I., and Williams, M. C. (2006) Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins Nucleic Acids Res. 34, 593-605 (Pubitemid 43240247)
7. Rein, A. (2010) Nucleic acid chaperone activity of retroviral Gag proteins RNA Biol. 7, 700-705
8. Levin, J. G., Guo, J. H., Rouzina, I., and 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. 80, 217-286 (Pubitemid 43574891)
9. Hargittai, M. R. S., Mangla, A. T., Gorelick, R. J., and Musier-Forsyth, K. (2001) 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, 985-997 (Pubitemid 32980320)
10. Khan, R. and Giedroc, D. P. (1992) Recombinant human immunodeficiency virus type 1 nucleocapsid (NCp7) protein unwinds tRNA J. Biol. Chem. 267, 6689-6695
11. Gregoire, C. J., Gautheret, D., and Loret, E. P. (1997) No tRNA3Lys unwinding in a complex with HIV NCp7 J. Biol. Chem. 272, 25143-25148 (Pubitemid 27415698)
12. 1H NMR study Nucleic Acids Res. 24, 3568-3575 (Pubitemid 26315769)
13. Chan, B. D., Weidemaier, K., Yip, W. T., Barbara, P. F., and Musier-Forsyth, K. (1999) Intra-tRNA distance measurements for nucleocapsid protein-dependent tRNA unwinding during priming of HIV reverse transcription Proc. Natl. Acad. Sci. U.S.A. 96, 459-464 (Pubitemid 29061230)
14. Hong, M. K., Harbron, E. J., OConnor, D. B., Guo, J. H., Barbara, P. F., Levin, J. G., and Musier-Forsyth, K. (2003) Nucleic acid conformational changes essential for HIV-1 nucleocapsid protein-mediated inhibition of self-priming in minus-strand transfer J. Mol. Biol. 325, 1-10 (Pubitemid 36152994)
15. Bernacchi, S., Stoylov, S., Piemont, E., Ficheux, D., Roques, B. P., Darlix, J. L., and Mely, Y. (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)
16. Cosa, G., Harbron, E. J., Zeng, Y. N., Liu, H. W., OConnor, D. B., Eta-Hosokawa, C., Musier-Forsyth, K., and Barbara, P. F. (2004) Secondary structure and secondary structure dynamics of DNA hairpins complexed with HIV-1 NC protein Biophys. J. 87, 2759-2767
17. Cosa, G., Zeng, Y. N., Liu, H. W., Landes, C. F., Makarov, D. E., Musier-Forsyth, K., and Barbara, P. F. (2006) Evidence for non-two-state kinetics in the nucleocapsid protein chaperoned opening of DNA hairpins J. Phys. Chem. B 110, 2419-2426 (Pubitemid 43342952)
18. Bourbigot, S., Ramalanjaona, N., Boudier, C., Salgado, G. F. J., Roques, B. P., Mely, Y., Bouaziz, S., and Morellet, N. (2008) How the HIV-1 Nucleocapsid Protein Binds and Destabilises the (-)Primer Binding Site During Reverse Transcription J. Mol. Biol. 383, 1112-1128
19. Rein, A., Feng, Y. X., Campbell, S., Harvin, D., Ehresmann, B., and Ehresmann, C. (1999) The human immunodeficiency virus type 1 Gag polyprotein has nucleic acid chaperone activity: Possible role in dimerization of genomic RNA and placement of tRNA on the primer binding site J. Virol. 73, 4251-4256 (Pubitemid 29189870)
20. Summers, M. F., Newman, J. L., Butcher, E. W., Patel, D. T., and Mikhaylenko, Y. (2004) Flexibility in the P2 domain of the HIV-1 Gag polyprotein Protein Sci. 13, 2101-2107 (Pubitemid 38989614)
21. Datta, S. A., Curtis, J. E., Ratcliff, W., Clark, P. K., Crist, R. M., Lebowitz, J., Krueger, S., and Rein, A. (2007) Conformation of the HIV-1 Gag protein in solution J. Mol. Biol. 365, 812-824 (Pubitemid 44960372)
22. Barklis, E., Alfadhli, A., and Still, A. (2009) Analysis of Human Immunodeficiency Virus Type 1 Matrix Binding to Membranes and Nucleic Acids J. Virol. 83, 12196-12203
23. Jones, C. P., Datta, S. A. K., Rein, A., Rouzina, I., and Musier-Forsyth, K. (2011) Matrix Domain Modulates HIV-1 Gags Nucleic Acid Chaperone Activity via Inositol Phosphate Binding J. Virol. 85, 1594-1603
24. Ward, D. C., Reich, E., and Stryer, L. (1969) Fluorescence Studies of Nucleotides and Polynucleotides. I. Formycin 2-Aminopurine Riboside 2,6-Diaminopurine Riboside and Their Derivatives J. Biol. Chem. 244, 1228-1237
25. Jean, J. M. and Hall, K. B. (2002) 2-Aminopurine electronic structure and fluorescence properties in DNA Biochemistry 41, 13152-13161 (Pubitemid 35244704)
26. Bradrick, T. D. and Marino, J. P. (2004) Ligand-induced changes in 2-aminopurine fluorescence as a probe for small molecule binding to HIV-1 TAR RNA RNA 10, 1459-1468 (Pubitemid 39122116)
27. Hall, K. B. and Williams, J. (2004) Dynamics of the IRE RNA hairpin loop probed by 2-aminopurine fluorescence and stochastic dynamics simulations RNA 10, 34-47 (Pubitemid 38018734)
28. Dibrov, S. M., Johnston-Cox, H., Weng, Y. H., and Hermann, T. (2007) Functional architecture of HCV IRES domain II stabilized by divalent metal ions in the crystal and in solution Angew. Chem., Int. Ed. 46, 226-229 (Pubitemid 46071706)
29. Godet, J., Ramalanjaona, N., Sharma, K. K., Richert, L., de Rocquigny, H., Darlix, J. L., Duportail, G., and Mely, Y. (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
30. Anderson, E. C. and Lever, A. M. (2006) Human immunodeficiency virus type 1 Gag polyprotein modulates its own translation J. Virol. 80, 10478-10486 (Pubitemid 44628894)
31. Swillens, S. (1995) Interpretation of Binding Curves Obtained with High Receptor Concentrations: Practical Aid for Computer Analysis Mol. Pharmacol. 47, 1197-1203
32. Sheehy, J. P., Davis, A. R., and Znosko, B. M. (2010) Thermodynamic characterization of naturally occurring RNA tetraloops RNA 16, 417-429
33. Antao, V. P., Lai, S. Y., and Tinoco, I. (1991) A Thermodynamic Study of Unusually Stable RNA and DNA Hairpins Nucleic Acids Res. 19, 5901-5905 (Pubitemid 21913002)
34. Blose, J. M., Proctor, D. J., Veeraraghavan, N., Misra, V. K., and Bevilacqua, P. C. (2009) Contribution of the Closing Base Pair to Exceptional Stability in RNA Tetraloops: Roles for Molecular Mimicry and Electrostatic Factors J. Am. Chem. Soc. 131, 8474-8484
35. Williams, D. J. and Hall, K. B. (2000) Experimental and computational studies of the G[UUCG]C RNA tetraloop J. Mol. Biol. 297, 1045-1061
36. Antao, V. P. and Tinoco, I. (1992) Thermodynamic parameters for loop formation in RNA and DNA hairpin tetraloops Nucleic Acids Res. 20, 819-824
37. Shubsda, M. F., Paoletti, A. C., Hudson, B. S., and Borer, P. N. (2002) Affinities of packaging domain loops in HIV-1 RNA for the nucleocapsid protein Biochemistry 41, 5276-5282 (Pubitemid 34411683)
38. Xi, X., Sun, Y., Karim, C. B., Grigoryants, V. M., and Scholes, C. P. (2008) HIV-1 nucleocapsid protein NCp7 and its RNA stem loop 3 partner: rotational dynamics of spin-labeled RNA stem loop 3 Biochemistry 47, 10099-10110
39. Shubsda, M. F., Kirk, C. A., Goodisman, J., and Dabrowiak, J. C. (2000) Binding of human immunodeficiency virus type 1 nucleocapsid protein to ψ-RNA-SL3 Biophys. Chem. 87, 149-165
40. Clever, J., Sassetti, C., and Parslow, T. G. (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
41. De Guzman, R. N., Wu, Z. R., Stalling, C. C., Pappalardo, L., Borer, P. N., and Summers, M. F. (1998) Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element Science 279, 384-388 (Pubitemid 28063374)
42. Maki, A. H., Ozarowski, A., Misra, A., Urbaneja, M. A., and Casas-Finet, J. R. (2001) Phosphorescence and optically detected magnetic resonance of HIV-1 nucleocapsid protein complexes with stem-loop sequences of the genomic ψ-recognition element Biochemistry 40, 1403-1412 (Pubitemid 32142902)
43. Shubsda, M. F., Paoletti, A. C., Hudson, B. S., and Borer, P. N. (2002) Affinities of packaging domain loops in HIV-1 RNA for the nucleocapsid protein Biochemistry 41, 5276-5282 (Pubitemid 34411683)
44. De Guzman, R. N., Wu, Z. R., Stalling, C. C., Pappalardo, L., Borer, P. N., and Summers, M. F. (1998) Structure of the HIV-1 nucleocapsid protein bound to the SL3 ψ-RNA recognition element Science 279, 384-388 (Pubitemid 28063374)
45. Vuilleumier, C., Bombarda, E., Morellet, N., Gerard, D., Roques, B. P., and Mely, Y. (1999) Nucleic acid sequence discrimination by the HIV-1 nucleocapsid protein NCp7: A fluorescence study Biochemistry 38, 16816-16825
46. Paoletti, A. C., Shubsda, M. F., Hudson, B. S., and Borer, P. N. (2002) Affinities of the nucleocapsid protein for variants of SL3 RNA in HIV-1 Biochemistry 41, 15423-15428 (Pubitemid 36008154)
47. Datta, S. A. K., Zhao, Z., Clark, P. K., Tarasov, S., Alexandratos, J. N., Campbell, S. J., Kvaratskhelia, M., Lebowitz, J., and Rein, A. (2007) Interactions between HIV-1 Gag molecules in solution: An inositol phosphate-mediated switch J. Mol. Biol. 365, 799-811 (Pubitemid 44960371)
48. Campbell, S. and Rein, A. (1999) In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain J. Virol. 73, 2270-2279 (Pubitemid 29098132)
49. Rambo, R. P. and Doudna, J. A. (2004) Assembly of an active group II intron-maturase complex by protein dimerization Biochemistry 43, 6486-6497 (Pubitemid 38697548)