Moloney murine sarcoma virus genomic RNAs dimerize via a two-step process: A concentration-dependent kissing-loop interaction is driven by initial contact between consecutive guanines

Journal of Virology

Volumn 73, Issue 9, 1999, Pages 7255-7261

  Ly, Hinh ^a   Nierlich, Donald P ^b   Olsen, John C ^a   Kaplan, Andrew H ^a,c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

ARTICLE; DIMERIZATION; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; PRIORITY JOURNAL; RNA STRUCTURE; VIRUS GENOME; VIRUS REPLICATION;

EID: 0032838983     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.9.7255-7261.1999     Document Type: Article

References (55)

1. Awang, G., and D. Sen. 1993. Mode of dimerization of HIV-1 genomic RNA. Biochemistry 32:11453-11457.
2. Baudin, F., R. Marquet, C. Isel, J.-L. Darlix, B. Ehresmann, and C. Ehresmann. 1993. Functional sites in the 5′ region of human immunodeficiency virus type 1 RNA from defined structural domains. J. Mol. Biol. 229:382-397.
3. Bender, W., Y.-H. Chien, S. Chattopadhyay, P. K. Vogt, M. B. Gardner, and N. Davidson. 1978. High-molecular-weight RNAs of AKR, NZB, and wild mouse viruses and avian reticuloendotheliosis virus all have similar dimer structures. J. Virol. 25:888-896.
4. Berkhout, B., and J. L. van Wamel. 1996. Role of the DIS hairpin in replication of human immunodeficiency virus type 1. J. Virol. 70:6723-6732.
5. Berkhout, B., B. B. Oude Essink, and I. Schneveld. 1993. In vitro dimerization of HIV-2 leader RNA in the absence of PuGGAPuA motifs. FASEB J. 7:181-187.
6. Cheong, C., and P. B. Moore. 1992. Solution structure of an unusually stable RNA tetraplex containing G- and U-quartet structures. Biochemistry 31: 8406-8414.
7. Clever, J. L., M. L. Wong, and T. G. Parslow. 1996. Requirements for kissing-loop-mediated dimerization of human immunodeficiency virus RNA. J. Virol. 70:5902-5908.
8. Clever, J. L., and T. G. Parslow. 1997. Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation. J. Virol. 71:3407-3414.
9. Darlix, J.-L. 1990. Cis elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J. Virol. 64:774-783.
10. Darlix, J.-L., C. Gabus, M.-T. Nugeyre, F. Clavel, and F. Barre-Sinoussi. 1990. cis elements and trans-acting factors involved in the RNA dimerization of the human immunodeficiency virus HIV-1. J. Mol. Biol. 216:689-699.
11. Doria-Rose N., and V. M. Vogt. 1998. In vivo selection of Rous sarcoma virus mutants with randomized sequences in the packaging signal. J. Virol. 72: 8073-8082.
12. Feng, Y. X., W. Fu, A. J. Winter, J. G. Levin, and A. Rein. 1995. Multiple regions of Harvey sarcoma virus RNA can dimerize in vitro. J. Virol. 69: 2486-2490.
13. Fu, W., and A. Rein. 1993. Maturation of dimeric viral RNA of Moloney murine leukemia virus. J. Virol. 67:5443-5449.
14. Fu, W., R. J. Gorelick, and A. Rein. 1994. Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and protease-defective virions. J. Virol. 68:5013-5018.
15. Gellert, M., M. N. Lipsett, and D. R. Davies. 1962. Helix formation by guanylic acid. Proc. Natl, Acad. Sci. USA 48:2013-2018.
16. Girard, P. M., B. Bonnet-Mathoniere, D. Muriaux, and J. Paoletti. 1995. A short autocomplementary sequence in the 5′ leader region is responsible for dimerization of MoMuLV genomic RNA. Biochemistry 34:9785-9794.
17. Girard, P. M., H. de Rocquigny, B. P. Roques, and J. Paoletti. 1996. A model of psi dimerization: destabilization of the C278-G303 stem-loop by the nucleocapsid protein (NCp10) of MoMuLV. Biochemistry 35:8705-8714.
18. Haddrick, M., A. L. Lear, A. J. Cann, and S. Heaphy. 1996. Evidence that a kissing loop structure facilitates genomic RNA dimerization in HIV-1. J. Mol. Biol. 259:58-68.
19. + in DNA quadruplexes is dominated by relative free energies of hydration: a thermodynamic analysis by 1H NMR. Biochemistry 35:15383-15390.
20. Kunkel, T. A., K. Bebenek, and J. McClary. 1991. Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 204:125-139.
21. Kung, H. J., S. Hu, W. Bender, J. M. Bailey, N. Davidson, M. O. Nicolson, and R. M. McAllister. 1976. RD-114, baboon, and wolly monkey viral RNAs compared in size and structure. Cell 7:609-620.
22. Laughlan, G., A. I. Murchie, D. G. Norman, M. H. Moore, P. C. Moody, D. M. Lilley, and B. Luisi. 1994. The high-resolution crystal structure of a parallel-stranded guanine tetraplex. Science 265:520-524.
23. Laughrea, M., and L. Jette. 1994. A 19-nucleotide sequence upstream of the 5′ major splice donor is part of the dimerization domain of human immunodeficiency virus 1 genomic RNA. Biochemistry 33:13464-13474.
24. Laughrea, M., L. Jette, J. Mak, L. Kleiman, C. Liang, and M. A. Wainberg. 1997. Mutations in the kissing-loop hairpin of human immunodeficiency virus type 1 reduce viral infectivity as well as genomic RNA packaging and dimerization. J. Virol. 71:3397-3406.
25. Lear, A. L., M. Haddrick, and S. Heaphy. 1995. A study of the dimerization of Rous sarcoma virus RNA in vitro and in vivo. Virology 212:47-57.
26. Louis, D. C., D. Gotte, E. Sanders-Buell, D. W. Ritchey, M. O. Salminen, J. K. Carr, and F. E. McCutchan. 1998. Infectious molecular clones with the nonhomologous dimer initiation sequences found in different subtypes of human immunodeficiency virus type 1 can recombine and initiate a spreading infection in vitro. J. Virol. 72:3991-3998.
27. Maisel, J., W. Bender, S. Hu, P. H. Duesberg, and N. Davidson. 1978. Structure of 50 to 70S RNA from Moloney sarcoma viruses. J. Virol. 25: 384-394.
28. Markowitz, D., S. Goff, and A. Bank. 1988. A safe packaging cell line for gene transfer: separating viral genes on two different plasmids. J. Virol. 62:1120-1124.
29. Marquet, R., F. Baudin, C. Gabus, J.-L. Darlix, M. Mougel, C. Ehresmann, and B. Ehresmann. 1991. Dimerization of human immunodeficiency virus (type 1) RNA: stimulation by cations and possible mechanism. Nucleic Acids Res. 91:2349-2357.
30. McBride, M. S., and A. T. Panganiban. 1996. The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J. Virol. 70:2963-2973.
31. McBride, M. S., M. D. Schwartz, and A. T. Panganiban. 1997. Efficient encapsidation of human immunodeficiency virus type 1 vectors and further characterization of cis elements required for encapsidation. J. Virol. 71: 4544-4554.
32. Adam, M. A., and D. Miller. 1988. Identification of a singnal in a murine retrovirus that is sufficient for packagaing of nonretroviral RNA into virions. J. Virol. 62:3802-3806.
33. Mougel, M., Y. Zhang, and E. Barklis. 1996. cis-active structural motifs involved in specific encapsidation of Moloney murine leukemia virus RNA. J. Virol. 70:5043-5050.
34. Muriaux, D., P.-M. Girard, B. Bonnet-Mathoniere, and J. Paoletti. 1995. Dimerization of HIV-1Lai RNA at low ionic strength: an autocomplementary sequence in the 5′ leader region is evidenced by an antisense oligonucleotide. J. Biol. Chem. 270:8209-8216.
35. Murti, K. G., M. Bondurant, and A. Tereba. 1981. Secondary structural features in the 70S RNAs of Moloney murine leukemia and Rous sarcoma viruses as observed by electron microscopy. J. Virol. 37:411-419.
36. Olsen, J. C. Unpublished data.
37. Olsen, J. C., and J. Sechelski. 1995. Use of sodium butyrate to enhance production of retroviral vectors expressing CFTR cDNA. Hum. Gene Ther. 6:1195-1202.
38. Paillart, J. C., R. Marquet, E. Skripkin, B. Ehresmann, and C. Ehresmann. 1994. Mutational analysis of the bipartite dimer linkage structure of human immunodeficiency virus type 1 genomic RNA. J. Biol. Chem. 269:27486-27493.
39. Paillart, J. C., L. Berthoux, M. Ottmann, J. L. Darlix, R. Marquet, B. Ehresmann, and C. Ehresmann. 1996. A dual role of the putative RNA dimerization initiation site of human immunodeficiency virus type 1 in genomic RNA packaging and proviral DNA synthesis. J. Virol. 70:8348-8354.
40. Paillart, J. C., R. Marquet, E. Skripkin, C. Ehresmann, and B. Ehresmann. 1996. Dimerization of retroviral genomic RNAs: structural and functional implications. Biochimie 78:639-653.
41. Paillart, J. C., E. Skripkin, B. Ehresmann, C. Ehresmann, and R. Marquet. 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.
42. Paoletti, J., M. Mougel, N. Tounekti, P. M. Girard, C. Ehresmann, and B. Ehresmann. 1993. Spontaneous dimerization of retroviral MoMuLV RNA. Biochimie 75:681-686.
43. Prats, A.-C., C. Roy, P. Wan, M. Erard, V. Housset, C. Gabus, C. Paoletti, and J. L. Darlix. 1990. cis-elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J. Virol. 64:774-783.
44. Reddy, P. E., M. J. Smith, and S. A. Aaroson. 1981. Complete nucleotide sequence and organization of the Moloney murine sarcoma virus genome. Science 214:445-450.
45. Sakuragi, J.-I., and A. T. Panganiban. 1997. Human immunodeficiency virus type 1 RNA outside the primary encapsidation and dimer linkage region affects RNA dimer stability in vivo. J. Virol. 71:3250-3254.
46. Skripkin, E., J. C. Paillart, R. Marquet, B. Ehresmann, and C. Ehresmann. 1994. Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proc. Natl. Acad. Sci. USA 91:4945-4949.
47. Stoltzfus, C. M., and P. N. Snyder. 1975. Structure of B77 sarcoma virus RNA: stabilization of RNA after packaging. J. Virol. 16:1161-1170.
48. Sundquist, W. I., and S. Heaphy. 1993. Evidence for interstrand quadruplex formation in the dimerization of human immunodeficiency virus type 1 genomic RNA. Proc. Natl. Acad. Sci. USA 90:3393-3397.
49. Tapia, M. D., V. Metzler, M. Mougel, B. Ehresmann, and C. Ehresmann. 1998. Dimerization of MoMuLV genomic RNA: redefinition of the role of the plaindromic stem-loop H1 (278-303) and new roles for stem-loops H2 (310-352) and H3 (355-374). Biochemistry 37:6077-6085.
50. Torrent, C., T. Bordet, and J. L. Darlix. 1994. Analytical study of rat retrotransposon VL30 RNA dimerization in vitro and packaging in murine leukemia virus. J. Mol. Biol. 240:434-444.
51. Torrent, C., C. Gabus, and J. L. Darlix. 1994. A small and efficient dimerization/packaging signal of rat VL30 RNA and its use in murine leukemia virus-VL30-derived vectors for gene transfer. J. Virol. 68:661-667.
52. Tounekti, N., M. Mougel, C. Roy, R. Marquet, J.-L. Darlix, J. Paoletti, B. Ehresmann, and C. Ehresmann. 1992. Effect of dimerization on the conformation of the encapsidation Psi domain of Moloney murine leukemia virus RNA. J. Mol. Biol. 223:205-220.
53. Wang, Y., and D. J. Patel. 1993. Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex. Structure 1:263-282.
54. Williamson, J. R., M. K. Raghuraman, and T. R. Cech. 1989. Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell 59: 871-880.
55. Zuker, M. 1989. On finding all suboptimal foldings of an RNA molecule. Science 244:48-52.