Composition and sequence-dependent binding of RNA to the nucleocapsid protein of moloney murine leukemia virus

Biochemistry

Volumn 44, Issue 10, 2005, Pages 3735-3744

  Dey, Anwesha ^a   York, Danielle ^a   Smalls Mantey, Adjoa ^a   Summers, Michael F ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; DIMERIZATION; ELECTROSTATICS; GENES; MATHEMATICAL MODELS; NUCLEAR MAGNETIC RESONANCE; RNA; TITRATION;

GENOME PACKAGING; NUCLEOCAPSID (NC) DOMAINS; RETROVIRUSES; REVERSE TRANSCRIPTION;

PROTEINS;

DIMER; GAG PROTEIN; GUANOSINE; NUCLEOCAPSID PROTEIN; OLIGONUCLEOTIDE;

ARTICLE; BINDING AFFINITY; DIMERIZATION; GENOME; ISOTHERMAL TITRATION CALORIMETRY; MOLONEY LEUKEMIA ONCOVIRUS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; RETROVIRUS; REVERSE TRANSCRIPTION; RNA ANALYSIS; RNA BINDING; RNA SEQUENCE; TITRIMETRY; VIRUS ASSEMBLY;

BASE COMPOSITION; BASE PAIRING; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; GENOME, VIRAL; GUANOSINE; HYDROPHOBICITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLONEY MURINE LEUKEMIA VIRUS; NUCLEOCAPSID PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PSEUDOURIDINE; RNA, VIRAL; RNA-BINDING PROTEINS; VIRUS ASSEMBLY; ZINC FINGERS;

MOLONEY MURINE LEUKEMIA VIRUS; MURINAE;

EID: 14844340022     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047639q     Document Type: Article

References (60)

1. Berkowitz, R., Fisher, J., and Goff, S. P. (1996) RNA packaging, Curr. Top. Microbiol. Immunol. 214, 177-218.
2. Hu, W.-S., and Temin, H. M. (1990) Genetic consequences of packaging two RNA genomes in one retroviral particle: Pseudodiploidy and high rate of genetic recombination, Proc. Natl. Acad. Sci. U.S.A. 87, 1556-1560.
3. Hu, W. S., and Temin, H. M. (1990) Retroviral recombination and reverse transcription, Science 250, 1227-1233.
4. Temin, H. M. (1991) Sex and recombination in retroviruses, Trends Genet. 7, 71-74.
5. Panganiban, A. T., and Fiore, D. (1988) Ordered interstrand and intrastrand DNA transfer during reverse transcription, Science 241, 1064-1069.
6. Jones, J. S., Allan, R. W., and Temin, H. M. (1993) Alteration of location of dimer linkage sequence in retroviral RNA: Little effect on replication or homologous recombination, J. Virol. 67, 3151-3158.
7. Mikkelsen, J. G., and Pedersen, F. S. (2000) Genetic reassortment and patch repair by recombination in retroviruses, J. Biomed. Sci. 7, 77-99.
8. Rein, A. (1994) Retroviral RNA packaging: A review, Arch. Virol. 9, 513-522.
9. Berkhout, B. (1996) Structure and function of the human immunodeficiency virus leader RNA, Prog. Nucleic Acid Res. Mol. Biol., 1-34.
10. Jewell, N. A., and Mansky, L. M. (2000) In the beginning: Genome recognition, RNA encapsidation and the initiation of complex retrovirus assembly, J. Gen. Virol. 81, 1889-1899.
11. Swanstrom, R., and Wills, J. W. (1997) in Retroviruses (Coffin, J. M., Hughes, S. H., and Varmus, H. E., Eds.) pp 263-334, Cold Spring Harbor Laboratory Press, Plainview, NY.
12. Stoker, A. W., and Bissell, M. J. (1988) Development of avian sarcoma and leukosis virus based vector packaging cell lines, J. Virol. 16, 1161-1170.
13. Mann, R., and Baltimore, D. (1985) Varying the position of a retrovirus packaging sequence results in the encapsidation of both unspliced and spliced RNA, J. Virol. 54, 401-407.
14. Watanabe, S., and Temin, H. M. (1982) Encapsidation sequences for spleen necrosis virus, an avian retrovirus, are between the 5′ long terminal repeat and the start of the gag gene, Proc. Natl. Acad. Sci. U.S.A. 79, 5986-5990.
15. Lever, A. M. L., Göttlinger, H. G., Haseltine, W. A., and Sodroski, J. G. (1989) Identification of a sequence required for efficient packaging of human immunodeficiency virus type 1 RNA into virions, J. Virol. 63, 4085-4087.
16. Aldovini, A., and Young, R. A. (1990) Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus, J. Virol. 64, 1920-1926.
17. Clavel, F., and Orenstein, J. M. (1990) A mutant of human immunodeficiency virus with reduced RNA packaging and abnormal particle morphology, J. Virol. 64, 5230-5234.
18. Poznansky, M., Lever, A. M. L., Bergeron, L., Haseltine, W., and Sodroski, J. (1991) Gene transfer into human lymphocytes by a defective human immunodeficiency virus type 1 vector, J. Virol. 65, 532-536.
19. Fisher, J., and Goff, S. P. (1998) Mutational analysis of stem-loops in the RNA packaging signal of the moloney murine leukemia virus, Virology 244, 133-145.
20. Mougel, M., Zhang, Y., and Barklis, E. (1996) cis-Active structural motifs involved in specific encapsidation of Moloney Murine leukemia virus RNA, J. Virol. 70, 5043-5050.
21. Mougel, M., and Barklis, E. (1997) A role for two hairpin structures as a core RNA encapsidation signal in murine leukemia virus virions, J. Virol. 71, 8061-8065.
22. Mansky, L. M., Krueger, A. E., and Temin, H. M. (1995) The bovine leukemia virus encapsidation signal is discontinuous and extends into the 5′ end of the gag gene, J. Virol. 69, 3282-3289.
23. Mansky, L. M., and Wisniewski, R. M. (1998) The bovine leukemia virus encapsidation signal is composed of RNA secondary structures, J. Virol. 72, 3196-3204.
24. McBride, M. S., and Panganiban, A. T. (1996) The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures, J. Virol. 70, 2963-2973.
25. Prats, A.-C., Roy, C., Wang, P., Erard, M., Housset, V., Gabus, C., Paoletti, C., and Darlix, J.-L. (1990) Cis elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA, J. Virol. 64, 774-783.
26. Housset, V., De Rocquigny, H., Roques, B. P., and Darlix, J.-L. (1993) Basic amino acids flanking the zinc finger of Moloney murine leukemia virus nucleocapsid protein NCp10 are critical for virus infectivity, J. Virol. 67, 2537-2545.
27. Levin, J. G., Grimley, P. M., Ramseur, J. M., and Berezesky, I. K. (1974) Deficiency of 60 to 70S RNA in murine leukemia virus particles assembled in cells treated with actinomycin D, J. Virol. 14, 152-161.
28. Paillart, J.-C., Shehu-Xhilaga, M., Marquet, R., and Mak, J. (2004) Dimerization of retroviral RNA genomes: An inseparable pair, Nat. Rev. Microbiol. 2, 461-472.
29. Kay, M. A., Liu, D., and Hoogerbrugge, P. M. (1997) Gene therapy, Proc. Natl. Acad. Sci. U.S.A. 94, 12744-12746.
30. Marcel, T., and Grausz, J. D. (1997) The TMC worldwide gene therapy enrollment report, end 1996, Hum. Gene Ther. 8, 775-800.
31. Yu, S. S., Kim, J.-M., and Kim, S. (2000) The 17 nucleotides downstream from the env gene stop codon are important for Murine Leukemia Virus packaging, J. Virol. 74, 8775-8780.
32. D'Souza, V., Dey, A., Habib, D., and Summers, M. F. (2004) NMR structure of the 101 nucleotide core encapsidation signal of the Moloney Murine Leukemia Virus, J. Mol. Biol. 337, 427-442.
33. D'Souza, V., Melamed, J., Habib, D., Pullen, K., Wallace, K., and Summers, M. F. (2001) Identification of a high-affinity nucleocapsid protein binding site within the Moloney Murine Leukemia Virus Ψ-RNA packaging signal. Implications for genome recognition, J. Mol. Biol. 314, 217-232.
34. D'Souza, V., and Summers, M. F. (2004) Structural basis for packaging the dimeric genome of Moloney Murine Leukaemia Virus, Nature 431, 586-590.
35. De Tapia, M., Metzler, V., Mougel, M., Ehresmann, B., and Ehresmann, C. (1998) Dimerization of MoMuLV genomic RNA: Redefinition of the role of the palindromic stem-loop H1 (278-303) and new roles for stem-loops H2 (310-352) and H3 (355-374), Biochemistry 37, 6077-6085.
36. Kim, C.-H., and Tinoco, I., Jr. (2000) A retroviral RNA kissing complex containing only two G-C base pairs, Proc. Natl. Acad. Sci. U.S.A. 97, 9396-9401.
37. Oroudjev, E. M., Kang, P. C. E., and Kohlstaedt, L. A. (1999) An additional dimer linkage structure in Moloney Murine Leukemia Virus RNA, J. Mol. Biol. 291, 603-613.
38. Ly, H., and Parslow, T. G. (2002) Bipartite signal for genomic RNA dimerization in the Moloney Murine Leukemia Virus, J. Virol. 76, 3135-3144.
39. South, T. L., and Summers, M. F. (1993) Zinc- and sequence-dependent binding to nucleic acids by the N-terminal zinc finger of the HIV-1 nucleocapsid protein: NMR structure of the complex with the ψ-site analog, dACGCC, Protein Sci. 2, 3-19.
40. 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.
41. Amarasinghe, G. K., De Guzman, R. N., Turner, R. B., Chancellor, K., Wu, Z.-R., and Summers, M. F. (2000) NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the Ψ-RNA packaging signal, J. Mol. Biol. 301, 491-511.
42. Tounekti, N., Mougel, M., Roy, C., Marquet, R., Darlix, J.-L., Paoletti, J., Ehresmann, B., and Ehresmann, C. (1992) Effect of dimerization on the conformation of the encapsidation ψ domain of Moloney murine leukemia virus RNA, J. Mol. Biol. 223, 205-220.
43. Mougel, M., Tounekti, N., Darlix, J.-L., Paoletti, J., Ehresmann, B., and Ehresmann, C. (1993) Conformational analysis of the 5′ leader and the gag initiation site of Mo-MuLV RNA and allosteric transitions induced by dimerization, Nucleic Acids Res. 21, 4677-4684.
44. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L.-N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter, Anal. Biochem. 179, 131-137.
45. Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) Investigation of exchange processes by two-dimensional NMR spectroscopy, J. Chem. Phys. 71, 4546-4553.
46. Macura, S., and Ernst, R. R. (1980) Elucidation of cross relaxation in liquids by two-dimensional NMR spectroscopy, Mol. Phys. 41, 95-117.
47. Bax, A., and Davis, D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy, J. Magn. Reson. 65, 355-360.
48. Braunschweiler, L., and Ernst, R. R. (1983) Coherence transfer by isotropic mixing: Application to proton correlation spectroscopy, J. Magn. Reson. 53, 521-528.
49. 1H spin system identification in macromolecules, J. Am. Chem. Soc. 110, 7870-7872.
50. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley & Sons, New York.
51. 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.
52. Johnson, B. A., and Blevins, R. A. (1994) NMRview: A Computer Program for the Visualization and Analysis of NMR Data, J. Biomol. NMR 4, 603-614.
53. Güntert, P., Mumenthaler, C., and Wuthrich, K. (1997) Torsion angle dynamics for protein structure calculations with a new program, DYANA, J. Mol. Biol. 273, 283-298.
54. Schuller, W., Dong, C.-Z., Wecker, K., and Roques, B.-P. (1999) NMR structure of the complex between the zinc finger protein NCp10 of Moloney Murine Leukemia Virus and the single-stranded pentanucleotide d(ACGCC): Comparison with HIV-NCp7 complexes, Biochemistry 38, 12984-12994.
55. Davis, J. T. (2004) G-Quartets 40 years later: From 5′-GMP to molecular biology and supramolecular chemistry, Angew. Chem. 43, 668-698.
56. Greatorex, J. (2004) The retroviral RNA dimer linkage: Different structures may reflect different roles, Retrovirology 1, Aug 18 issue.
57. Russell, R. S., Liang, C., and Wainberg, M. A. (2004) Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably? Retrovirology 1, Sept 2 issue.
58. Nisole, S., and Saib, A. (2004) Early steps of retrovirus replicative cycle, Retrovirology 1, May 14 issue.
59. Mann, R., Mulligan, R. C., and Baltimore, D. (1983) Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus, Cell 33, 153-159.
60. Bender, M. A., Palmer, T. D., Gelinas, R. E., and Miller, A. D. (1987) Evidence that the packaging signal of Moloney murine leukemia virus extends into the gag region, J. Virol. 61, 1639-1646.