Molecular determinants of HIV-1 NCp7 chaperone activity in maturation of the HIV-1 dimerization initiation site

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages 2565-2580

  Aduri, Raviprasad ^a   Briggs, Katharine T ^a   Gorelick, Robert J ^b   Marino, John P ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINOPURINE; AMINO ACID; CHAPERONE; DIMER; NCP7 CHAPERONE; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; COMPARATIVE STUDY; DIMERIZATION; DIMERIZATION INITIATION SITE; DNA FLANKING REGION; FLUORESCENCE; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA TRANSPORT; VIRUS GENOME; ZINC FINGER MOTIF;

2-AMINOPURINE; AMINO ACID SEQUENCE; DIMERIZATION; FLUORESCENCE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; RNA, VIRAL; ZINC FINGERS;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84876361672     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1350     Document Type: Article

References (78)

1. Paillart, J.C., Marquet, R., Skripkin, E., Ehresmann, C. and Ehresmann, B. (1996) Dimerization of retroviral genomic RNAs: structural and functional implications. Biochimie, 78, 639-653.
2. Miele, G., Mouland, A., Harrison, G.P., Cohen, E. and Lever, A.M. (1996) The human immunodeficiency virus type 1 5' packaging signal structure affects translation but does not function as an internal ribosome entry site structure. J. Virol., 70, 944-951.
3. 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.
4. Clever, J.L., Miranda, D. Jr. and Parslow, T.G. (2002) RNA structure and packaging signals in the 5' leader region of the human immunodeficiency virus type 1 genome. J. Virol., 76, 12381-12387.
5. Berkowitz, R.D. and Goff, S.P. (1994) Analysis of binding elements in the human immunodeficiency virus type 1 genomic RNA and nucleocapsid protein. Virology, 202, 233-246.
6. Harrison, G.P., Miele, G., Hunter, E. and Lever, A.M. (1998) Functional analysis of the core human immunodeficiency virus type 1 packaging signal in a permissive cell line. J. Virol., 72, 5886-5896.
7. McBride, M.S., Schwartz, M.D. and Panganiban, A.T. (1997) Efficient encapsidation of human immunodeficiency virus type 1 vectors and further characterization of cis elements required for encapsidation. J. Virol., 71, 4544-4554.
8. Sakaguchi, K., Zambrano, N., Baldwin, E.T., Shapiro, B.A., Erickson, J.W., Omichinski, J.G., Clore, G.M., Gronenborn, A.M. and Appella, E. (1993) Identification of a binding site for the human immunodeficiency virus type 1 nucleocapsid protein. Proc. Natl Acad. Sci. USA, 90, 5219-5223.
9. Paillart, J.C., Skripkin, E., Ehresmann, B., Ehresmann, C. and Marquet, R. (1996) A loop-loop ''kissing'' complex is the essential part of the dimer linkage of genomic HIV-1 RNA. Proc. Natl Acad. Sci. USA, 93, 5572-5577.
10. Paillart, J.C., Westhof, E., Ehresmann, C., Ehresmann, B. and Marquet, R. (1997) Non-canonical interactions in a kissing loop complex: the dimerization initiation site of HIV-1 genomic RNA. J. Mol. Biol., 270, 36-49.
11. Laughrea, M. and Jette, L. (1996) Kissing-loop model of HIV-1 genome dimerization: HIV-1 RNAs can assume alternative dimeric forms, and all sequences upstream or downstream of hairpin 248-271 are dispensable for dimer formation. Biochemistry, 35, 1589-1598.
12. Jossinet, F., Paillart, J.C., Westhof, E., Hermann, T., Skripkin, E., Lodmell, J.S., Ehresmann, C., Ehresmann, B. and Marquet, R. (1999) Dimerization of HIV-1 genomic RNA of subtypes A and B: RNA loop structure and magnesium binding. RNA, 5, 1222-1234.
13. Weixlbaumer, A., Werner, A., Flamm, C., Westhof, E. and Schroeder, R. (2004) Determination of thermodynamic parameters for HIV DIS type loop-loop kissing complexes. Nucleic Acids Res., 32, 5126-5133.
14. Takahashi, K.I., Baba, S., Chattopadhyay, P., Koyanagi, Y., Yamamoto, N., Takaku, H. and Kawai, G. (2000) Structural requirement for the two-step dimerization of human immunodeficiency virus type 1 genome. RNA, 6, 96-102.
15. Muriaux, D., De Rocquigny, H., Roques, B.P. and Paoletti, J. (1996) NCp7 activates HIV-1Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. J. Biol. Chem., 271, 33686-33692.
16. Rist, M.J. and Marino, J.P. (2002) Mechanism of nucleocapsid protein catalyzed structural isomerization of the dimerization initiation site of HIV-1. Biochemistry, 41, 14762-14770.
17. Mujeeb, A., Ulyanov, N.B., Georgantis, S., Smirnov, I., Chung, J., Parslow, T.G. and James, T.L. (2007) Nucleocapsid protein-mediated maturation of dimer initiation complex of full-length SL1 stemloop of HIV-1: sequence effects and mechanism of RNA refolding. Nucleic Acids Res., 35, 2026-2034.
18. Rein, A., Henderson, L.E. and Levin, J.G. (1998) Nucleic-Acidchaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem. Sci., 23, 297-301.
19. Feng, Y.X., Copeland, T.D., Henderson, L.E., Gorelick, R.J., Bosche, W.J., Levin, J.G. and Rein, A. (1996) HIV-1 nucleocapsid protein induces ''maturation'' of dimeric retroviral RNA in vitro. Proc. Natl Acad. Sci. USA, 93, 7577-7581.
20. Lapadat-Tapolsky, M., De Rocquigny, H., Van Gent, D., Roques, B., Plasterk, R. and Darlix, J.L. (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.
21. Druillennec, S., Caneparo, A., de Rocquigny, H. and Roques, B.P. (1999) Evidence of interactions between the nucleocapsid protein NCp7 and the reverse transcriptase of HIV-1. J. Biol. Chem., 274, 11283-11288.
22. Peliska, J.A., Balasubramanian, S., Giedroc, D.P. and Benkovic, S.J. (1994) Recombinant HIV-1 nucleocapsid protein accelerates HIV-1 reverse transcriptase catalyzed DNA strand transfer reactions and modulates RNase H activity. Biochemistry, 33, 13817-13823.
23. Wu, W., Henderson, L.E., Copeland, T.D., Gorelick, R.J., Bosche, W.J., Rein, A. and Levin, J.G. (1996) Human immunodeficiency virus type 1 nucleocapsid protein reduces reverse transcriptase pausing at a secondary structure near the murine leukemia virus polypurine tract. J. Virol., 70, 7132-7142.
24. Johnson, P.E., Turner, R.B., Wu, Z.R., Hairston, L., Guo, J., Levin, J.G. and Summers, M.F. (2000) A mechanism for plus-strand transfer enhancement by the HIV-1 nucleocapsid protein during reverse transcription. Biochemistry, 39, 9084-9091.
25. Guo, J., Wu, T., Kane, B.F., Johnson, D.G., Henderson, L.E., Gorelick, R.J. and Levin, J.G. (2002) 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, 4370-4378.
26. Guo, J., Wu, T., Anderson, J., Kane, B.F., Johnson, D.G., Gorelick, R.J., Henderson, L.E. and Levin, J.G. (2000) Zinc finger structures in the human immunodeficiency virus type 1 nucleocapsid protein facilitate efficient minus-and plus-strand transfer. J. Virol., 74, 8980-8988.
27. Darlix, J.L., Godet, J., Ivanyi-Nagy, R., Fosse, P., Mauffret, O. and Mely, Y. (2011) Flexible nature and specific functions of the HIV-1 nucleocapsid protein. J. Mol. Biol., 410, 565-581.
28. Berkhout, B., Gorelick, R., Summers, M.F., Mely, Y. and Darlix, J.L. (2008) 6th international symposium on retroviral nucleocapsid. Retrovirology, 5, 21.
29. Summers, M.F., Henderson, L.E., Chance, M.R., Bess, J.W. Jr., South, T.L., Blake, P.R., Sagi, I., Perez-Alvarado, G., Sowder, R.C. 3rd, Hare, D.R. et al. (1992) Nucleocapsid zinc fingers detected in retroviruses: EXAFS studies of intact viruses and the solution-state structure of the nucleocapsid protein from HIV-1. Protein Sci., 1, 563-574.
30. Lee, B.M., De Guzman, R.N., Turner, B.G., Tjandra, N. and Summers, M.F. (1998) Dynamical behavior of the HIV-1 nucleocapsid protein. J. Mol. Biol., 279, 633-649.
31. Morellet, N., Jullian, N., De Rocquigny, H., Maigret, B., Darlix, J.L. and Roques, B.P. (1992) Determination of the structure of the nucleocapsid protein NCp7 from the human immunodeficiency virus type 1 by 1H NMR. EMBO J., 11, 3059-3065.
32. Amarasinghe, G.K., De Guzman, R.N., Turner, R.B., Chancellor, K.J., Wu, Z.R. and Summers, M.F. (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.
33. 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.
34. Morellet, N., Demene, H., Teilleux, V., Huynh-Dinh, T., de Rocquigny, H., Fournie-Zaluski, M.C. and Roques, B.P. (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.
35. Mori, M., Dietrich, U., Manetti, F. and Botta, M. (2010) Molecular dynamics and DFT study on HIV-1 nucleocapsid protein-7 in complex with viral genome. J. Chem. Inf. Model, 50, 638-650.
36. Kafaie, J., Song, R., Abrahamyan, L., Mouland, A.J. and Laughrea, M. (2008) Mapping of nucleocapsid residues important for HIV-1 genomic RNA dimerization and packaging. Virology, 375, 592-610.
37. Gorelick, R.J., Nigida, S.M. Jr, Bess, J.W. Jr., Arthur, L.O., Henderson, L.E. and Rein, A. (1990) Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. J. Virol., 64, 3207-3211.
38. Gorelick, R.J., Chabot, D.J., Rein, A., Henderson, L.E. and Arthur, L.O. (1993) The two zinc fingers in the human immunodeficiency virus type 1 nucleocapsid protein are not functionally equivalent. J. Virol., 67, 4027-4036.
39. Drummond, J.E., Mounts, P., Gorelick, R.J., Casas-Finet, J.R., Bosche, W.J., Henderson, L.E., Waters, D.J. and Arthur, L.O. (1997) Wild-type and mutant HIV type 1 nucleocapsid proteins increase the proportion of long cDNA transcripts by viral reverse transcriptase. AIDS Res. Hum. Retroviruses, 13, 533-543.
40. Hargittai, M.R., 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.
41. Buckman, J.S., Bosche, W.J. and Gorelick, R.J. (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.
42. Wu, T., Datta, S.A., 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.
43. Mirambeau, G., Lyonnais, S. and Gorelick, R.J. (2010) Features, processing states, and heterologous protein interactions in the modulation of the retroviral nucleocapsid protein function. RNA Biol., 7, 85-95.
44. Feng, Y.X., Campbell, S., Harvin, D., Ehresmann, B., Ehresmann, C. and Rein, A. (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.
45. De Rocquigny, H., Gabus, C., Vincent, A., Fournie-Zaluski, M.C., Roques, B. and Darlix, J.L. (1992) 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, 6472-6476.
46. Thomas, J.A., Gagliardi, T.D., Alvord, W.G., Lubomirski, M., Bosche, W.J. and Gorelick, R.J. (2006) Human immunodeficiency virus type 1 nucleocapsid zinc-finger mutations cause defects in reverse transcription and integration. Virology, 353, 41-51.
47. Kanevsky, I., Chaminade, F., Ficheux, D., Moumen, A., Gorelick, R., Negroni, M., Darlix, J.L. and Fossé, P. (2005) Specific interactions between HIV-1 nucleocapsid protein and the TAR element. J. Mol. Biol., 348, 1059-1077.
48. Takahashi, K., Baba, S., Koyanagi, Y., Yamamoto, N., Takaku, H. and Kawai, G. (2001) Two basic regions of NCp7 are sufficient for conformational conversion of HIV-1 dimerization initiation site from kissing-loop dimer to extended-duplex dimer. J. Biol. Chem., 276, 31274-31278.
49. Baba, S., Takahashi, K., Koyanagi, Y., Yamamoto, N., Takaku, H., Gorelick, R.J. and Kawai, G. (2003) Role of the zinc fingers of HIV-1 nucleocapsid protein in maturation of genomic RNA. J. Biochem., 134, 637-639.
50. Dannull, J., Surovoy, A., Jung, G. and Moelling, K. (1994) Specific binding of HIV-1 nucleocapsid protein to PSI RNA in vitro requires N-terminal zinc finger and flanking basic amino acid residues. EMBO J., 13, 1525-1533.
51. Urbaneja, M.A., Kane, B.P., Johnson, D.G., Gorelick, R.J., Henderson, L.E. and Casas-Finet, J.R. (1999) 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, 59-75.
52. Dorfman, T., Luban, J., Goff, S.P., Haseltine, W.A. and Gottlinger, H.G. (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.
53. Turner, K.B., Hagan, N.A. and Fabris, D. (2007) Understanding the isomerization of the HIV-1 dimerization initiation domain by the nucleocapsid protein. J.Mol.Biol., 369, 812-828.
54. Hagan, N.A. and Fabris, D. (2007) Dissecting the protein-RNA and RNA-RNA interactions in the nucleocapsid-mediated dimerization and isomerization of HIV-1 stemloop 1. J. Mol. Biol., 365, 396-410.
55. Mihailescu, M.R. and Marino, J.P. (2004) A proton-coupled dynamic conformational switch in the HIV-1 dimerization initiation site kissing complex. Proc. Natl Acad. Sci. USA, 101, 1189-1194.
56. Lee, H.W., Briggs, K.T. and Marino, J.P. (2009) Dissecting structural transitions in the HIV-1 dimerization initiation site RNA using 2-Aminopurine fluorescence. Methods, 49, 118-127.
57. Beaucage, S.L. and Caruthers, M.H. (1981) Deoxynucleoside phosphoramidites-A new class of key intermediates for deoxypolynucleotide synthesis. Tetrahedron Lett., 22, 1859-1862.
58. Stampfl, S., Lempradl, A., Koehler, G. and Schroeder, R. (2007) Monovalent ion dependence of neomycin B binding to an RNA aptamer characterized by spectroscopic methods. Chembiochem, 8, 1137-1145.
59. Menne, S., Asif, G., Narayanasamy, J., Butler, S.D., George, A.L., Hurwitz, S.J., Schinazi, R.F., Chu, C.K., Cote, P.J., Gerin, J.L. et al. (2007) Antiviral effect of orally administered (-)-beta-D-2-aminopurine dioxolane in woodchucks with chronic woodchuck hepatitis virus infection. Antimicrob. Agents Chemother., 51, 3177-3184.
60. Carteau, S., Gorelick, R.J. and Bushman, F.D. (1999) Coupled integration of human immunodeficiency virus type 1 cDNA ends by purified integrase in vitro: stimulation by the viral nucleocapsid protein. J. Virol., 73, 6670-6679.
61. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
62. Goddard, T.D. and Kneller, D.G. SPARKY 3. University of California, San Francisco.
63. Fisher, R.J., Fivash, M.J., Stephen, A.G., Hagan, N.A., Shenoy, S.R., Medaglia, M.V., Smith, L.R., Worthy, K.M., Simpson, J.T., Shoemaker, R. et al. (2006) Complex interactions of HIV-1 nucleocapsid protein with oligonucleotides. Nucleic Acids Res., 34, 472-484.
64. Schmalzbauer, E., Strack, B., Dannull, J., Guehmann, S. and Moelling, K. (1996) Mutations of basic amino acids of NCp7 of human immunodeficiency virus type 1 affect RNA binding in vitro. J. Virol., 70, 771-777.
65. Avilov, S.V., Godet, J., Piemont, E. and Mely, Y. (2009) Site-specific characterization of HIV-1 nucleocapsid protein binding to oligonucleotides with two binding sites. Biochemistry, 48, 2422-2430.
66. Avilov, S.V., Piemont, E., Shvadchak, V., de Rocquigny, H. and Mely, Y. (2008) Probing dynamics of HIV-1 nucleocapsid protein/ target hexanucleotide complexes by 2-Aminopurine. Nucleic Acids Res., 36, 885-896.
67. 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.
68. 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.
69. Demene, H., Dong, C.Z., Ottmann, M., Rouyez, M.C., Jullian, N., Morellet, N., Mely, Y., Darlix, J.L., Fournie-Zaluski, M.C., Saragosti, S. et al. (1994) 1H NMR structure and biological studies of the His23-Cys mutant nucleocapsid protein of HIV-1 indicate that the conformation of the first zinc finger is critical for virus infectivity. Biochemistry, 33, 11707-11716.
70. Stote, R.H., Kellenberger, E., Muller, H., Bombarda, E., Roques, B.P., Kieffer, B. and Mely, Y. (2004) Structure of the His44-Ala single point mutant of the distal finger motif of HIV-1 nucleocapsid protein: a combined NMR, molecular dynamics simulation, and fluorescence study. Biochemistry, 43, 7687-7697.
71. Morellet, N., de Rocquigny, H., Mely, Y., Jullian, N., Demene, H., Ottmann, M., Gerard, D., Darlix, J.L., Fournie-Zaluski, M.C. and Roques, B.P. (1994) Conformational behaviour of the active and inactive forms of the nucleocapsid NCp7 of HIV-1 studied by 1H NMR. J. Mol. Biol., 235, 287-301.
72. Bourbigot, S., Ramalanjaona, N., Boudier, C., Salgado, G.F., 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.
73. Mujeeb, A., Clever, J.L., Billeci, T.M., James, T.L. and Parslow, T.G. (1998) Structure of the dimer initiation complex of HIV-1 genomic RNA. Nat. Struct. Bio, 5, 432-436.
74. Baba, S.T.K., Noguchi, S., Takaku, H., Koyanagi, Y., Yamamoto, N. and Kawai, G. (2005) Solution RNA structures of the HIV-1 dimerization initiation site in the kissing-loop and extended-duplex dimers. J. Biochem., 138, 583-592.
75. Kieken, F., Paquet, F., Brulé, F., Paoletti, J. and Lancelot, G. (2006) A new NMR solution structure of the SL1 HIV-1Lai loop-loop dimer. Nucleic Acids Res., 34, 343-352.
76. Ennifar, E., Walter, P., Ehresmann, B., Ehresmann, C. and Dumas, P. (2001) Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site. Nat. Struct. Biol, 8, 1064-1068.
77. Mujeeb, A., Parslow, T.G., Zarrinpar, A., Das, C., James, T.L., Clever, J.L. and Billeci, T.M. (1999) NMR structure of the mature dimer initiation complex of HIV-1 genomic RNA. FEBS Lett., 458, 387-392.
78. Ennifar, E., Yusupov, M., Walter, P., Marquet, R., Ehresmann, B., Ehresmann, C. and Dumas, P. (1999) The crystal structure of the dimerization initiation site of genomic HIV-1 RNA reveals an extended duplex with two adenine bulges. J. Mol. Biol., 7, 1439-1449.