Dimerization of retroviral RNA genomes: An inseparable pair

Nature Reviews Microbiology

Volumn 2, Issue 6, 2004, Pages 461-472

  Paillart, Jean Christophe ^a   Shehu Xhilaga, Miranda ^b   Marquet, Roland ^a   Mak, Johnson ^b,c  

^a INST DE BIOL MOLEC ET CELLULAIRE   (France)

^b BURNET INSTITUTE   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; NUCLEIC ACID; VIRUS RNA;

DIMERIZATION; GENE MUTATION; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; RETROVIRUS; REVERSE TRANSCRIPTION; REVIEW; RNA CONFORMATION; RNA GENE; RNA PROCESSING; RNA STABILITY; RNA STRUCTURE; RNA TRANSPORT; THERMOSTABILITY; VIRAL GENETICS; VIRION; VIRUS ASSEMBLY; VIRUS REPLICATION; CHEMICAL STRUCTURE; CONFORMATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; VIRUS GENOME;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES; UNIDENTIFIED RETROVIRUS;

BASE SEQUENCE; DIMERIZATION; GENOME, VIRAL; HIV-1; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; VIRUS REPLICATION;

EID: 2942657412     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro903     Document Type: Review

References (156)

1. Bender, W. & Davidson, N. Mapping of poly(A) sequences in the electron microscope reveals unusual structure of type C oncornavirus RNA molecules. Cell 7, 595-607 (1976).
2. Bender, W. et al. 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 (1978).
3. Kung, H. J. et al. RD-114, baboon, and woolly monkey viral RNAs compared in size and structure. Cell 7, 609-620 (1976).
4. Murti, K. G., Bondurant, M. & Tereba, A. 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 (1981).
5. Roy, C. et al. An analytical study of the dimerization of in vitro generated RNA of Moloney murine leukemia virus MoMuLV. Nucleic Acids Res. 18, 7287-7292 (1990).
6. Marquet, R. et al. Dimerization of human immunodeficiency virus (Type 1) RNA: stimulation by cations and possible mechanism. Nucleic Acids Res. 19, 2349-2357 (1991).
7. Darlix, J. L., Gabus, C., Nugeyre, M. T., Clavel, F. & Barre-Sinoussi, F. Cis elements and trans-acting factors involved in the RNA dimerization of the human immunodeficiency virus HIV-1. J. Mol. Biol. 216, 689-99 (1990).
8. Skripkin, E., Paillart, J.-C., Marquet, R., Ehresmann, B. & Ehresmann, C. Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proc. Natl Acad. Sci. USA 91, 4945-4949 (1994).
9. Paillart, J.-C., Marquet, R., Skripkin, E., Ehresmann, B. & Ehresmann, C. Mutational analysis of the bipartite dimer linkage structure of human immunodeficiency virus type 1 genomic RNA. J. Biol. Chem. 269, 27486-27493 (1994).
10. Laughrea, M. & Jette, L. 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 (1994).
11. Clever, J. L., Wong, M. L. & Parslow, T. G. Requirements for kissing-loop-mediated dimerization of human immunodeficiency virus RNA. J. Virol. 70, 5902-5908 (1996).
12. Lai 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 (1995).
13. Lai. RNA dimerization process in vitro. Biochemistry 35, 5075-5082 (1996).
14. Paillart, J.-C., Westhof, E., Ehresmann, C., Ehresmann, B. & Marquet, R. Non-canonical interactions in a kissing loop complex: the dimerization initation site of HIV-1 genomic RNA. J. Mol. Biol. 270, 36-49 (1997).
15. Paillart, J.-C., Skripkin, E., Ehresmann, B., Ehresmann, C. & Marquet, R. 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 (1996).
16. Laughrea, M., Shen, N., Jetté, L. & Wainberg, M. A. Variant effects of non-native kissing-loop hairpin palindromes on HIV-1 replication and HIV RNA dimerzation. Biochemistry 38, 226-234 (1999).
17. Lodmell, J. S., Ehresmann, C., Ehresmann, B. & Marquet, R. Convergence of natural and artificial evolution on an RNA loop-loop interaction: the HIV-1 dimerization initiation site, RNA 6, 1267-1276 (2000).
18. Lodmell, J. S., Ehresmann, C., Ehresmann, B. & Marquet, R. Structure and dimerization of HIV-1 kissing loop aptamers. J. Mol. Biol. 311, 475-490 (2001).
19. Jossinet, F., Lodmell, J. S., Ehresmann, C., Ehresmann, B. & Marquet, R. Identification of the in vitro HIV-2/SIV RNA dimerization site reveals striking differences with HIV-1. J. Biol. Chem. 276, 5598-5604 (2001).
20. Ennifar, E., Walter, P., Ehresmann, B., Ehresmann, C. & Dumas, P. Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site. Nature Struct. Biol. 8, 1064-1068 (2001).
21. Lai genomic RNA: NMR solution structure of the extended duplex, J. Biomol. Struct. Dyn. 16, 1145-1157 (1999).
22. Mujeeb, A., Clever, J. L., Billeci, T. M., James, T. L. & Parslow, T. G. Structure of the dimer initiation complex of HIV-1 genomic RNA. Nature Struct. Biol. 5, 432-436 (1998).
23. Ennifar, E. et al. The crystal structure of the dimerization initiation site of genomic HIV-1 RNA reveals an extended duplex with two adenine bulges. Structure Fold. Des. 7, 1439-1449 (1999).
24. Mujeeb, A., Parslow, T. G., Zarrinpar, A., Das, C. & James, T. L. NMR structure of the mature dimer initiation complex of HIV-1 genomic RNA. FEBS Lett. 458, 387-392 (1999).
25. Lai RNA dimerization. Thermodynamic parameters associated with the transition from the kissing complex to the extended dimer. Eur. J. Biochem. 267, 2711-2719 (2000).
26. Rist, M. J. & Marino, J. P. Mechanism of nucleocapsid protein catalyzed structural isomerization of the dimerization initiation site of HIV-1. Biochemistry 41, 14762-14770 (2002).
27. Mihailescu, M. R. & Marino, J. P. A proton-coupled dynamic conformational switch in the HIV-1 dimerization initiation site kissing complex. Proc. Natl Acad. Sci. USA 101, 1189-1194 (2004).
28. Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. J. Biol. Chem. 271, 33686-33692 (1996).
29. Feng, Y.-X. et al. HIV-1 nucleocapsid protein induces 'maturation' of dimeric retroviral RNA in vitro. Proc. Natl Acad. Sci. USA 93, 7577-7581 (1996).
30. Prats, A. C. et al. cis elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J. Virol. 64, 774-783 (1990).
31. Takahashi, K. I. et al. Structural requirement for the two-step dimerization of human immunodeficiency virus type 1 genome. RNA 6, 96-102 (2000).
32. Laughrea, M. & Jetté, L. Kissing-loop model of HIV-1 genomic dimerization: HIV-1 RNAs can assume alternative dimeric forms, and all sequences upstream or downstream of hairpin 248-271 are dispensable for dimeric formation. Biochemistry 35, 1589-1598 (1996).
33. Lanchy, J. M., Ivanovitch, J. D. & Lodmell, J, S. A structural linkage between the dimerization and encapsidation signals in HIV-2 leader RNA. RNA 9, 1007-1018 (2003).
34. Marquet, R., Paillart, J.-C., Skripkin, E., Ehresmann, C. & Ehresmann, B. Dimerization of human immunodeficiency virus type 1 RNA involves sequences located upstream of the splice donor site. Nucleic Acids Res. 22, 145-151 (1994).
35. Laughrea, M. & Jette, L. HIV-1 genome dimerization: kissing-loop hairpin dictates whether nucleotides downstream of the 5′ splice junction contribute to loose and tight dimerization of human immunodeficiency virus RNA. Biochemistry 36, 9501-9508 (1997).
36. Stewart, L., Schatz, G. & Vogt, V. M. Properties of avian retrovirus particles defective in viral protease. J. Virol. 64, 5076-5092 (1990).
37. Oertle, S. & Spahr, P. F. Role of the gag polyprotein precursor in packaging and maturation of Rous sarcoma virus genomic RNA. J. Virol. 64, 5757-5763 (1990).
38. Fu, W. & Rein, A. Maturation of dimeric viral RNA of Moloney murine leukemia virus. J. Virol. 67, 5443-5449 (1993).
39. Fu, W., Gorelick, R. J. & Rein, A. Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and protease-defective virions. J. Virol. 68, 5013-5018 (1994).
40. Feng, Y.-X., Moore, S. P., Garfinkel, D. J. & Rein, A. The genomic RNA in Ty1 virus-like particles is dimeric. J. Virol. 74, 10819-10821 (2000).
41. Feng, Y.-X. et al. 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 (1999).
42. Shen, N., Jetté, L., Liang, C., Wainberg, M. A. & Laughrea, M. Impact of human immunodeficiency virus type 1 RNA dimerization on viral infectivity and of stem-loop B on RNA dimerization and reverse transcription and dissociation of dimerization from packaging. J. Virol. 74, 5729-5735 (2000).
43. Pattabiraman, N., Martinez, H. M. & Shapiro, B. A. Molecular modeling and dynamics studies of HIV-1 kissing loop structures. J. Biomol. Struct. Dyn. 20, 397-412 (2002).
44. Paillart, J. C., Skripkin, E., Ehresmann, B., Ehresmann, C. & Marquet, R. In vitro evidence for a long range pseudoknot in the 5′-untranslated and matrix coding regions of HIV-1 genomic RNA. J. Biol. Chem. 277, 5995-6004 (2002).
45. Abbink, T. E. & Berkhout, B. A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the gag start codon. J. Biol. Chem. 278, 11601-1111 (2003).
46. Berkhout, B. et al. In vitro evidence that the untranslated leader of the HIV-1 genome as an RNA checkpoint that regulates multiple functions through conformational changes. J. Biol. Chem. 277, 19967-19975 (2002).
47. Berkhout, B. & van Wamel, J. L. B. The leader of the HIV-1 RNA genome forms a compactly folded tertiary structure. RNA 6, 282-295 (2000).
48. Huthoff, H. & Berkhout, B. Mutations in the TAR hairpin affect the equilibrium between alternative conformations of the HIV-1 leader RNA. Nucleic Acids Res. 29, 2594-2600 (2001).
49. Huthoff, H. & Berkhout, B. Two alternating structures of the HIV-1 leader RNA. RNA 7, 143-157 (2001).
50. Lanchy, J. M. & Lodmell, J. S. Alternate usage of two dimerization initiation sites in HIV-2 viral RNA in vitro. J. Mol. Biol. 319, 637-648 (2002).
51. Lanchy, J. M., Rentz, C. A., Ivanovitch, J. D. & Lodmell, J. S. Elements located upstream and downstream of the major splice donor site influence the ability of HIV-2 leader RNA to dimerize in vitro. Biochemistry 42, 2634-2642 (2003).
52. Andersen, E. S. et al. Role of the TAR hairpin in dimerization of HIV-1 RNA. J. Biol. Chem. (Mar 2004) doi: 10.1074/jbc.M314326200.
53. Höglund, S., Öhagen, A., Goncalves, J., Panganiban, A. T. & Gabuzda, D. Ultrstructure of HIV-1 genomic RNA. Virology 233, 271-279 (1997).
54. Brasey, A. et al. The leader of human immunodeficiency virus type 1 genomic RNA harbors an internal ribosome entry segment that is active during the G2/M phase of the cell cycle. J. Virol. 77, 3939-3949 (2003).
55. Dirac, A. M., Huthoff, H., Kjems, J. & Berkhout, B. The dimer initiation site hairpin mediates dimerization of the human immunodeficiency virus, type 2 RNA genome. J. Biol. Chem. 276, 32345-32352 (2001).
56. Le Blanc, I., Greatorex, J., Dokhelar, M. C. & Lever, A. M. A 37-base sequence in the leader region of human T-cell leukaemia virus type I is a high affinity dimerization site but is not essential for virus replication. J. Gen. Virol. 81, S105-S108 (2000).
57. Monie, T., Greatorex, J. & Lever, A. M. Oligonucleotide mapping of the core genomic RNA dimer linkage in human T-cell leukaemia virus type-1. Virus Res. 78, 45-56 (2001).
58. Greatorex, J. S., Laisse, V., Dokhelar, M.-C. & Lever, A. M. L. Sequences involved in the dimerisation of human T cell leukaemia virus type-1 RNA. Nucleic Acids Res. 24, 2919-2923 (1996).
59. Erlwein, O., Cain, D., Fischer, N., Rethwilm, A. & McClure, M. O. Identification of sites that act together to direct dimerization of human foamy virus RNA in vitro. Virology 229, 251-258 (1997).
60. Cain, D., Erlwein, O., Grigg, A., Russell, R. A. & McClure, M. O. Palindromic sequence plays a critical role in human foamy virus dimerization. J. Virol. 75, 3731-3739 (2001).
61. Park, J. & Mergia, A. Mutational analysis of the 5′ leader region of simian foamy virus type 1. Virology 274, 203-212 (2000).
62. Katoh, I., Kyushiki, H., Sakamoto, Y., Ikawa, Y. & Yoshinaka, Y. Bovine leukemia virus matrix-associated protein MA(p15): further processing and formation of a specific complex with the dimer of the 5′-terminal genomic RNA fragment. J. Virol. 65, 6845-6855 (1991).
63. Katoh, I., Yesunaga, T. & Yoshinaka, Y. Bovine leukemia virus RNA sequences involved in dimerization and specific Gag protein binding: close relation to the packaging site of avian, murine, and human retroviruses. J. Virol. 67, 1830-1839 (1993).
64. Polge, E., Darlix, J. L., Paoletti, J. & Fosse, P. Characterization of loose and tight dimer forms of avian leukosis virus RNA. J. Mol. Biol. 300, 41-56 (2000).
65. Fosse, P. et al. A short autocomplementary sequence plays an essential role in avian sarcoma-leukosis virus RNA dimerization. Biochemistry 35, 16601-16609 (1996).
66. Bieth, E., Gabus, C. & Darlix, J.-L. A study of the dimer formation of Rous sarcoma virus RNA and of its effect on viral protein synthesis in vitro. Nucleic Acids Res. 18, 119-127 (1990).
67. Darlix, J. L., Gabus, C. & Allain, B. Analytical study of avian reticuloendotheliosis virus dimeric RNA generated in vivo and in vitro. J. Virol. 66, 7245-7252 (1992).
68. Lear, A. L., Haddrick, M. & Heaphy, S. A study of the dimerization of Rous sarcoma virus RNA in vitro and in vivo. Virology 212, 47-57 (1995).
69. Torrent, C., Gabus, C. & Darlix, J. L. 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 (1994).
70. Girard, P.-M., Bonnet-Mathonière, B., Muriaux, D. & Paoletti, J. A short autocomplementary sequence in the 5′ leader region is responsible for dimerization of MoMuLV genomic RNA. Biochemistry 34, 9785-9794 (1995).
71. Oroudjev, E. M., Kang, P. C. & Kohlstaedt, L. A. An additional dimer linkage structure in Moloney murine leukemia virus RNA. J. Mol. Biol. 291, 603-613 (1999).
72. Ly, H., Nierlich, D. P., Olsen, J. C. & Kaplan, A. H. Moloney murine sarcoma virus genomic RNAs dimerize via a two-step process: a concentration-dependent kissing-loop interaction is driven by initial contact between conscutive guanines. J. Virol. 73, 7255-7261 (1999).
73. Ly, H., Nierlich, D. P., Olsen, J. C. & Kaplan, A. H. Functional characterization of the dimer linkage structure RNA of Moloney murine sarcoma virus. J. Virol. 74, 9937-9945 (2000).
74. Ly, H. & Parslow, T. G. Bipartite signal for genomic RNA dimerization in Moloney murine leukemia virus. J. Virol. 76, 3135-3144 (2002).
75. De Tapia, M., Metzler, V., Mougel, M., Ehresmann, B. & Ehresmann, C. 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 (1998).
76. Dirac, A. M., Huthoff, H., Kjems, J. & Berkhout, B. Regulated HIV-2 RNA dimerization by means of alternative RNA conformations. Nucleic Acids Res. 30, 2647-2655 (2002).
77. Rasmussen, S. V., Mikkelsen, J. G. & Pedersen, F. S. Modulation of homo- and heterodimerization of Harvey sarcoma virus RNA by GACG tetraloops and point mutations in palindromic sequences. J. Mol. Biol. 323, 613-628 (2002).
78. Kim, C. H. & Tinoco, I. Jr. A retroviral RNA kissing complex containing only two GC base pairs. Proc. Natl Acad. Sci. USA 97, 9396-9401 (2000).
79. Berkhout, B. & van Wamel, J. L. B. Role of the DIS hairpin in replication of human immunodeficiency virus type 1. J. Virol. 70, 6723-6732 (1996).
80. Clever, J. L. & Parslow, T. G. Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation. J. Virol. 71, 3407-3414 (1997).
81. Haddrick, M., Lear, A. L., Cann, A. J. & Heaphy, S. Evidence that a kissing loop structure facilitates genomic RNA dimerisation in HIV-1. J. Mol. Biol. 259, 58-68 (1996).
82. Laughrea, M. et al. 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 (1997).
83. Liang, C. et al. Deletion mutagenesis within the dimerization initation site of human immunodeficiency virus type 1 results in delayed processing of the p2 peptide from precursor proteins. J. Virol. 73, 6147-6151 (1999).
84. Liang, C. et al. Mutations within four distinct Gag proteins are required to restore replication of human immunodeficiency virus type 1 after deletion mutagenesis within the dimerization initation site. J. Virol. 73, 7014-7020 (1999).
85. Paillart, J. C. et al. A dual role of the putative RNA dimerization initation site of human immunodeficiency virus type 1 in genomic RNA packaging and proviral DNA synthesis. J. Virol. 70, 8348-8354 (1996).
86. Russell, R. S. et al. Effects of a single amino acid substitution within the p2 region of human immunodeficiency virus type 1 on packaging of spliced viral RNA. J. Virol. 77, 12986-12995 (2003).
87. Ortiz-Conde, B. A. & Hughes, S. H. Studies of the genomic RNA of leukosis viruses: implications for RNA dimerization. J. Virol. 73, 7165-7174 (1999).
88. Sakuragi, J.-I. & Panganiban, A. T. Human immunodeficiency virus type 1 RNA outside the primary encapsidation and dimer linkage region affects RNA dimer stability in vitro. J. Virol. 71, 3250-3254 (1997).
89. Berkhout, B. Structure and function of the human immunodeficiency virus leader RNA. Prog. Nucleic Acid Res. Mol. Biol. 54, 1-34 (1996).
90. Shen, N., Jette, L., Wainberg, M. A. & Laughrea, M. Role of stem B, loop B, and nucleotides next to the primer binding site and the kissing-loop domain in human immunodeficiency virus type 1 replication and genomic-RNA dimerization. J. Virol. 75, 10543-10549 (2001).
91. Hill, M. K. et al. The dimer initiation sequence stem-loop of human immunodeficiency virus type 1 is dispensable for viral replication in peripheral blood mononuclear cells. J. Virol. 77, 8329-8335 (2003).
92. Russell, R. S. et al. Sequences downstream of the 5′ splice donor site are required for both packaging and dimerization of human immunodeficiency virus type 1 RNA. J. Virol. 77, 84-96 (2003).
93. Russell, R. S., Hu, J., Laughrea, M., Weinberg, M. A. & Liang, C. Deficient dimerization of human immunodeficiency virus type 1 RNA caused by mutations of the U5 RNA sequences. Virology 303, 152-163 (2002).
94. Sakuragi, J., Ueda, S., Iwamoto, A. & Shioda, T. Possible role of dimerization in human immunodeficiency virus type 1 genome RNA packaging. J. Virol. 77, 4060-4069 (2003).
95. Rong, L. et al. Deletion of stem loop 3 is compensated by second-site mutations within the Gag protein of human immunodeficiency virus type 1. Virology 314, 221-228 (2003).
96. Cen, S. et al. The role of Pr55(gag) in the annealing of tRNALys3 to human immunodeficiency virus type 1 genomic RNA. J. Virol. 73, 4485-4488 (1999).
97. Rong, L. et al. Roles of the human immunodeficiency virus type 1 nucleocapsid protein in annealing and initation versus elongation in reverse transcription of viral negative-strand strong-stop DNA. J. Virol. 72, 9353-9358 (1998).
98. Cen, S. et al. Roles of Pr55(gag) and NCp7 in tRNA(3)(Lys) genomic placement and the initiation step of reverse transcription in human immunodeficiency virus type 1. J. Virol. 74, 10796-10800 (2000).
99. Gabus, C. et al. The yeast Ty3 retrotransposon contains a 5′-3′ bipartite primer-binding site and encodes nucleocapsid protein NCp9 functionally homologous to HIV-1 NCp7. EMBO J. 17, 4873-4880 (1998).
100. Cristofari, G., Ficheux, D. & Darlix, J. L. The GAG-like protein of the yeast Ty1 retrotransposon contains a nucleic acid chaperone domain analogous to retroviral nucleocapsid proteins. J. Biol. Chem. 275, 19210-19217 (2000).
101. Berkhout, B., Das, A. T. & van Wamel, J. L. The native structure of the human immunodeficiency virus type 1 RNA genome is required for the first strand transfer of reverse transcription. Virology 249, 211-218 (1998).
102. Cheung, K. S., Smith, R. E., Stone, M. P. & Joklik, W. K. Comparison of immature (rapid harvest) and mature Rous sarcoma virus particles. Virology 50, 851-864 (1972).
103. Canaani, E., Helm, K. V. D. & Duesberg, P. Evidence for the 30-40S RNA as precursor of the 60-70S RNA of Rous sarcoma virus. Proc. Natl Acad. Sci. USA 70, 401-405 (1973).
104. Levin, J. G., Grimley, P. M., Ramseur, J. M. & Berezesky, I. K. Deficiency of 60 to 70S RNA in murine leukemia virus particles assembled in cells treated with actinomycin D. J. Virol. 14, 152-161 (1974).
105. McBride, M. S. & Panganiban, A. T. Position dependence of functional hairpins important for human immunodeficiency virus type 1 RNA encapsidation in vivo. J. Virol. 71, 2050-2058 (1997).
106. McBride, M. S. & Panganiban, A. T. The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J. Virol. 70, 2963-2973 (1996).
107. Harrison, G. P., Miele, G., Hunter, E. & Lever, A. M. Functional analysis of the core human immunodeficiency virus type 1 packaging signal in a permissive cell line. J. Virol. 72, 5886-5896 (1998).
108. Parent, L. J. et al. RNA dimerization defect in a Rous sarcoma virus matrix mutant. J. Virol. 74, 164-172 (2000).
109. Garbitt, R. A., Albert, J. A., Kessler, M. D. & Parent, L. J. Trans-acting inhibition of genomic RNA dimerization by Rous sarcoma virus matrix mutants. J. Virol. 75, 260-268 (2001).
110. Sakuragi, J., Iwamoto, A. & Shioda, T. Dissociation of genome dimerization from packaging functions and virion maturation of human immunodeficiency virus type 1. J. Virol. 76, 959-967 (2002).
111. Sakuragi, J., Shioda, T. & Panganiban, A. T. Duplication of the primary encapsidation and dimer linkage region of human immunodeficiency virus type 1 RNA results in the appearance of monomeric RNA in virions. J. Virol. 75, 2557-2565 (2001).
112. Shehu-Xhilaga, M., Crowe, S. M. & Mak, J. Maintenance of the Gag/Gag-Pol ratio is important for human immunodeficiency virus type 1 RNA dimerization and viral infectivity. J. Virol. 75, 1834-1841 (2001).
113. Dupont, S. et al. A novel nuclear export activity in HIV-1 matrix protein required for viral replication. Nature 402, 681-685 (1999).
114. Scheifele, L. Z., Garbitt, R. A., Rhoads, J. D. & Parent, L. J. Nuclear entry and CRM1-dependent nuclear export of the Rous sarcoma virus Gag polyprotein. Proc. Natl Acad. Sci. USA 99, 3944-3949 (2002).
115. Mouland, A. J. et al. RNA trafficking signals in human immunodeficiency virus type 1. Mol. Cell. Biol. 21, 2133-2143 (2001).
116. Mouland, A. J. et al. The double-stranded RNA-binding protein Staufen is incorporated in human immunodeficiency virus type 1: evidence for a role in genomic RNA encapsidation. J. Virol. 74, 5441-5451 (2000).
117. Chatel-Chaix, L. et al. Identification of Staufen in the human immunodeficiency virus type 1 Gag ribonucleoprotein complex and a role in generating infectious viral particles. Mol. Cell. Biol. 24, 2637-2648 (2004).
118. Ferrandon, D., Koch, I., Westhof, E. & Nusslein-Volhard, C. RNA-RNA interaction is required for the formation of specific bicoid mRNA 3′ UTR-STAUFEN ribonucleoprotein particles. EMBO J. 16, 1751-1758 (1997).
119. Freed, F. O. HIV-1 Gag proteins: diverse functions in the virus life cycle. Virology 251, 1-15 (1998).
120. Freed, E. O. The HIV-TSG101 interface: recent advances in a budding field. Trends Microbiol. 11, 56-59 (2003).
121. Kaplan, A. H., Manchester, M. & Swanstrom, R. The activity of the protease of human immunodeficiency virus type 1 is initiated at the membrane of infected cells before the release to occur with maximum efficiency. J. Virol. 68, 6782-6786 (1994).
122. Gottlinger, H. G., Sodroski, J. G. & Haseltine, W. A. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc. Natl Acad. Sci. USA 86, 5781-5785 (1989).
123. Katoh, I. et al. Murine leukemia virus mutation: protease region required for conversion from 'immature' to 'mature' core form and for virus infectivity. Virology 145, 280-292 (1985).
124. Campbell, S. & Vogt, V. M. In vitro assembly of virus-like particles with Rous sarcoma virus gag deletion mutants: identification of the p10 domain as a morphological determinant in the formation of spherical particles. J. Virol. 71, 4425-4435 (1997).
125. Campbell, S. & Vogt, V. M. Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1. J. Virol. 69, 6487-6497 (1995).
126. Campbell, S. & Rein, A. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol. 73, 2270-2279 (1999).
127. Muriaux, D., Mirro, J., Harvin, D. & Rein, A. RNA is a structural element in retroviral particles. Proc. Natl Acad. Sci. USA 98, 5246-5251 (2001).
128. Wang, S. W., Noonan, K. & Aldovini, A. Nucleocapsid-RNA interactions are essential to structural stability but not to assembly of retroviruses. J. Virol. 78, 716-723 (2004).
129. Stoltzfus, C. M. & Snyder, P. N. Structure of B77 sarcoma virus RNA: stabilization of RNA after packaging. J. Virol. 64, 1161-1170 (1975).
130. Pettit, S. C., Sheng, N., Tritch, R., Erickson-Vitanen, S. & Swanstrom, R. The regulation of sequential processing of HIV-1 Gag by the viral protease. Adv. Exp. Med. Biol. 436, 15-25 (1998).
131. Shehu-Xhilaga, M. et al. Proteolytic processing of the p2/nucleocapsid cleavage site is critical for human immunodeficiency virus type 1 RNA dimer maturation. J. Virol. 75, 9156-9164 (2001).
132. Oshima, M. et al. Effects of blocking individual maturation cleavages in murine leukemia virus Gag. J. Virol. 78, 1411-1420 (2004).
133. Sheng, N. et al. Determinants of the human immunodeficiency virus type 1 p15NC-RNA interaction that affect enhanced cleavage by the viral protease. J. Virol. 71, 5723-5732 (1997).
134. Liang, C., Rong, L., Laughrea, M., Kleiman, L. & Wainberg, M. A. Compensatory point mutations in the human immunodeficiency virus type 1 Gag region that are distal from deletion mutations in the dimerization initation site can restore viral replication. J. Virol. 72, 6629-6636 (1998).
135. Panganiban, A. T. & Fiore, D. Ordered interstrand and intrastrand DNA transfer during reverse transcription. Science 241, 1064-1069 (1988).
136. Hu, W. S. & Temin, H. M. Retroviral recombination and reverse transcription. Science 250, 1227-1233 (1990).
137. van Wamel, J. L. & Berkhout, B. The first strand transfer during HIV-1 reverse transcription can occur either intramolecularly or intermolecularly. Virology 244, 245-251 (1998).
138. Temin, H. M. Sex and recombination in retroviruses. Trends Genet. 7, 71-74 (1991).
139. Mikkelsen, J. G., Lund, A. H., Duch, M. & Pedersen, F. S. Recombination in the 5′ leader of murine leukemia virus is accurate and influenced by sequence identity with a strong bias toward the kissing-loop dimerization region. 72, 6967-6978 (1998).
140. Mikkelsen, J. G., Lund, A. H., Dybkaer, K., Duch, M. & Pedersen, F. S. Extended minus-strand DNA as template for R-U5-mediated second-strand transfer in recombinational rescue of prime binding site-modified retroviral vectors. J. Virol. 72, 2519-2525 (1998).
141. Mikkelsen, J. G. et al. A preferred region for recombinational patch repair in the 5′ untranslated region of primer binding site-impaired murine leukemia virus vectors. J. Virol. 70, 1439-1447 (1996).
142. Mikkelsen, J. G., Lund, A. H., Duch, M. & Pedersen, F. S. Mutations of the kissing-loop dimerization sequence influence the site specificity of murine leukemia virus recombination in vivo. J. Virol. 74, 600-610 (2000).
143. Lund, A. H., Mikkelsen, J. G., Schmidt, J., Duch, M. & Pedersen, F. S. The kissing-loop motif is a preferred site of 5′ leader recombination during replication of SL3-3 murine leukemia viruses in mice. J. Virol. 73, 9614-9618 (1999).
144. Balakrishnan, M., Fay, P. J. & Bambara, R. A. The kissing hairpin sequence promotes recombination within the HIV-I 5′ leader region. J. Biol. Chem. 276, 36482-36492 (2001).
145. Balakrishnan, M., Roques, B. P., Fay, P. J. & Bambara, R. A. Template dimerization promotes an acceptor invasion-induced transfer mechanism during human immunodeficiency virus type 1 minus-strand synthesis. J. Virol. 77, 4710-4721 (2003).
146. Andersen, E. S., Jeeninga, R. E., Damgaard, C. K., Berkhout, B. & Kjems, J. Dimerization and template switching in the 5′ untranslated region between various subtypes of human immunodeficiency virus type 1. J. Virol. 77, 3020-3030 (2003).
147. Piyasirisilp, S. et al. A recent outbreak of human immunodeficiency virus type 1 infection in southern China was initiated by two highly homogeneous, geographically separated strains, circulating recombinant form AE and a novel BC recombinant. J. Virol. 74, 11286-11295 (2000).
148. Su, L. et al. Characterization of a virtually full-length human immunodeficiency virus type 1 genome of a prevalent intersubtype (C/B′) recombinant strain in China. J. Virol. 74, 11367-11376 (2000).
149. Moutouh, L., Corbeil, J. & Richman, D. D. Recombination leads to the rapid emergence of HIV-1 dually resistant mutants under selective drug pressure. Proc. Natl Acad. Sci. USA 93, 6106-6111 (1996).
150. Yusa, K., Kavlick, M. F., Kosalaraksa, P. & Mitsuya, H. HIV-1 acquires resistance to two classes of antiviral drugs through homologous recombination. Antiviral. Res. 36, 179-189 (1997).
151. Jung, A. et al. Multiply infected spleen cells in HIV patients. Nature 418, 144 (2002).
152. Dang, Q. et al. Nonrandom HIV-1 infection and double infection via direct and cell-mediated pathways. Proc. Natl Acad. Sci. USA 101, 632-637 (2004).
153. Levy, D. N., Aldrovandi, G. M., Kutsch, O. & Shaw, G. M. Dynamics of HIV-1 recombination in its natural target cells. Proc. Natl Acad. Sci. USA 101, 4204-4209 (2004).
154. Ennifar, E. et al. HIV-1 RNA dimerization initiation site is structurally similar to the ribosomal A site and binds aminoglycoside antibiotics. J. Biol. Chem. 278, 2723-2730 (2003).
155. McPike, M. P., Sullivan, J. M., Goodisman, J. & Dabrowiak, J. C. Footprinting, circular dichroism and UV melting studies on neomycin B binding to the packaging region of human immunodeficiency virus type-1 RNA. Nucleic Acids Res. 30, 2825-2831 (2002).
156. Kim, H. J., Lee, K. & O'Rear, J. J. A short sequence upstream of the 5′ splice site is important for encapsidation of HIV-1 genomic RNA. Virology 198, 336-340 (1994).