Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably?

Retrovirology

Volumn 1, Issue , 2004, Pages

  Russell, Rodney S ^a,b   Liang, Chen ^a,c   Wainberg, Mark A ^a,b,c  

^a MCGILL UNIVERSITY   (Canada)

^b Dept of Microbiology and Immunology ^*  (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE ANTIBIOTIC AGENT; AMINOSALICYLIC ACID; ANTIRETROVIRUS AGENT; DIMER; GENOMIC RNA; NEOMYCIN; RNA 16S; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN; VIRUS RNA; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT;

COVALENT BOND; DIMERIZATION; DNA VECTOR; DRUG TARGETING; GENE STRUCTURE; GENETIC CONSERVATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LIFE CYCLE; RETROVIRUS; REVIEW; RNA INTERFERENCE; RNA SPLICING; RNA STRUCTURE; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS GENOME; VIRUS REPLICATION; DRUG DESIGN; GENETICS; METABOLISM; PHYSIOLOGY;

ANTI-HIV AGENTS; DIMERIZATION; DRUG DESIGN; GENOME, VIRAL; HIV-1; RNA, VIRAL;

EID: 14844359526     PISSN: 17424690     EISSN: None     Source Type: Journal    
DOI: 10.1186/1742-4690-1-23     Document Type: Review

References (136)

1. Greatorex J, Lever A: Retroviral RNA dimer linkage. J Gen Virol 1998, 79(Pt 12):2877-2882.
2. Paillart JC, Marquet R, Skripkin E, Ehresmann C, Ehresmann B: Dimerization of retroviral genomic RNAs: structural and functional implications. Biochimie 1996, 78:639-653.
3. Berkhout B: Structure and function of the human immunodeficiency virus leader RNA. Prog Nucleic Acid Res Mol Biol 1996, 54:1-34.
4. Lever AM, Richardson JH, Harrison GP: Retroviral RNA packaging. Biochem Soc Trans 1991, 19:963-966.
5. Lever AM: HIV RNA packaging and lentivirus-based vectors. Adv Pharmacol 2000, 48:1-28.
6. Berkowitz R, Fisher J, Goff SP: RNA packaging. Curr Top Microbiol Immunol 1996, 214:177-218.
7. Rein A: Retroviral RNA packaging: a review. Arch Virol Suppl 1994, 9:513-522.
8. Rein A, Henderson LE, Levin JG: Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem Sci 1998, 23:297-301.
9. Katz RA, Jentoft JE: What is the role of the cys-his motif in retroviral nucleocapsid (NC) proteins? Bioessays 1989, 11: 176-181.
10. Paillart JC, Shehu-Xhilaga M, Marquet R, Mak J: Dimerization of retroviral RNA genomes: an inseparable pair. Nat Rev Microbiol 2004, 2:461-472.
11. Greatorex J: The retroviral RNA dimer linkage: different structures may reflect diiferent roles. Retrovirology 2004, 1:22.
12. Robinson WS, Robinson HL, Duesberg PH: Tumor virus RNA's. Proc Natl Acad Sci U S A 1967, 58:825-834.
13. Duesberg PH: Physical properties of Rous Sarcoma Virus RNA. Proc Natl Acad Sci U S A 1968, 60:1511-1518.
14. Kung HJ, Bailey JM, Davidson N, Nicolson MO, McAllister RM: Structure, subunit composition, and molecular weight of RD-114 RNA. J Virol 1975, 16:397-411.
15. Bender W, Davidson N: Mapping of poly(A) sequences in the electron microscope reveals unusual structure of type C oncornavirus RNA molecules. Cell 1976, 7:595-607.
16. Kung HJ, Hu S, Bender W, Bailey JM, Davidson N, Nicolson MO, McAllister RM: RD-114, baboon, and woolly monkey viral RNA's compared in size and structure. Cell 1976, 7:609-620.
17. Dube S, Kung HJ, Bender W, Davidson N, Ostertag W: Size, subunit composition, and secondary structure of the Friend virus genome. J Virol 1976, 20:264-272.
18. Maisel J, Bender W, Hu S, Duesberg PH, Davidson N: Structure of 50 to 70S RNA from Moloney sarcoma viruses. J Virol 1978, 25:384-394.
19. Bender W, Chien YH, Chattopadhyay S, Vogt PK, Gardner MB, Davidson N: High-molecular-weight RNAs of AKR, NZB, and wild mouse viruses and avian reticuloendotheliosis virus all have similar dimer structures. J Virol 1978, 25:888-896.
20. Gonda MA, Rice NR, Gilden RV: Avian reticuloendotheliosis virus: characterization of the high-molecular-weight viral RNA in transforming and helper virus populations. J Virol 1980, 34: 743-751.
21. Murti KG, 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 1981, 37: 411-419.
22. Khandjian EW, Meric C: A procedure for Northern blot analysis of native RNA. Anal Biochem 1986, 159:227-232.
23. Darlix JL, Gabus C, Nugeyre MT, 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 1990, 216:689-699.
24. Meric C, Spahr PF: Rous sarcoma virus nucleic acid-binding protein p12 is necessary for viral 70S RNA dimer formation and packaging. J Virol 1986, 60:450-459.
25. Marquet R, Paillart JC, 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 1994, 22:145-151.
26. Skripkin E, Paillart JC, 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 U S A 1994, 91:4945-4949.
27. 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 1994, 33: 13464-13474.
28. Muriaux D, Girard PM, Bonnet-Mathoniere B, Paoletti J: Dimerization of HIV-1 Lai RNA at low ionic strength. An autocomplementary sequence in the 5′ leader region is evidenced by an antisense oligonucleotide. J Biol Chem 1995, 270:8209-8216.
29. Paillart JC, 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 U S A 1996, 93:5572-5577.
30. 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. Nat Struct Biol 2001, 8: 1064-1068.
31. Mujeeb A, Parslow TG, Zarrinpar A, Das C, James TL: NMR structure of the mature dimer initiation complex of HIV-1 genomic RNA. FEBS Lett 1999, 458:387-392.
32. Laughrea M, Jette L, Mak J, Kleiman L, Liang C, Wainberg MA: 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 1997, 71:3397-3406.
33. Berkhout B, van Wamel JL: Role of the DIS hairpin in replication of human immunodeficiency virus type 1. J Virol 1996, 70:6723-6732.
34. Polge E, Darlix JL, Paoletti J, Fosse P: Characterization of loose and tight dimer forms of avian leukosis virus RNA. J Mol Biol 2000, 300:41-56.
35. Fosse P, Motte N, Roumier A, Gabus C, Muriaux D, Darlix JL, Paoletti J: A short autocomplementary sequence plays an essential role in avian sarcoma-leukosis virus RNA dimerization. Biochemistry 1996, 35:16601-16609.
36. 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 1998, 37: 6077-6085.
37. Girard PM, de Rocquigny H, Roques BP, Paoletti J: A model of PSI dimerization: destabilization of the C278-G303 stem-loop by the nucleocapsid protein (NCp10) of MoMuLV. Biochemistry 1996, 35:8705-8714.
38. Girard PM, Bonnet-Mathoniere B, Muriaux D, Paoletti J: A short autocomplementary sequence in the 5′ leader region is responsible for dimerization of MoMuLV genomic RNA. Biochemistry 1995, 34:9785-9794.
39. Tounekti N, Mougel M, Roy C, Marquet R, Darlix JL, Paoletti J, Ehresmann B, Ehresmann C: Effect of dimerization on the conformation of the encapsidation Psi domain of Moloney murine leukemia virus RNA. J Mol Biol 1992, 223:205-220.
40. Jossinet F, Lodmell JS, 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 2001, 276: 5598-5604.
41. Dirac AM, 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 2001, 276:32345-32352.
42. Fu W, Rein A: Maturation of dimeric viral RNA of Moloney murine leukemia virus. J Virol 1993, 67:5443-5449.
43. Feng YX, Copeland TD, Henderson LE, Gorelick RJ, Bosche WJ, Levin JG, Rein A: HIV-1 nucleocapsid protein induces "maturation" of dimeric retroviral RNA in vitro. Proc Natl Acad Sci U S A 1996, 93:7577-7581.
44. Muriaux D, De Rocquigny H, Roques BP, Paoletti J: NCp7 activates HIV-1 Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. J Biol Chem 1996, 271: 33686-33692.
45. Laughrea M, Shen N, Jette L, Darlix JL, Kleiman L, Wainberg MA: Role of distal zinc finger of nucleocapsid protein in genomic RNA dimerization of human immunodeficiency virus type 1; no role for the palindrome crowning the R-U5 hairpin. Virology 2001, 281: 109-116.
46. Hu WS, Temin HM: 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 1990, 87: 1556-1560.
47. Andersen ES, Jeeninga RE, Damgaard CK, Berkhout B, Kjems J: Dimerization and template switching in the 5′ untranslated region between various subtypes of human immunodeficiency virus type 1. J Virol 2003, 77:3020-3030.
48. Balakrishnan M, Fay PJ, Bambara RA: The kissing hairpin sequence promotes recombination within the HIV-I 5′ leader region. J Biol Chem 2001, 276:36482-36492.
49. Balakrishnan M, Roques BP, Fay PJ, Bambara RA: Template dimerization promotes an acceptor invasion-induced transfer mechanism during human immunodeficiency virus type 1 minus-strand synthesis. J Virol 2003, 77:4710-4721.
50. van Wamel JL, Berkhout B: The first strand transfer during HIV-1 reverse transcription can occur either intramolecularly or intermolecularly. Virology 1998, 244:245-251.
51. Aldovini A, Young RA: Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus. J Virol 1990, 64:1920-1926.
52. Clavel F, Orenstein JM: A mutant of human immunodeficiency virus with reduced RNA packaging and abnormal particle morphology. J Virol 1990, 64:5230-5234.
53. Lever A, Gottlinger H, Haseltine W, Sodroski J: Identification of a sequence required for efficient packaging of human immunodeficiency virus type 1 RNA into virions. J Virol 1989, 63:4085-4087.
54. Adam MA, Miller AD: Identification of a signal in a murine retrovirus that is sufficient for packaging of nonretroviral RNA into virions. J Virol 1988, 62:3802-3806.
55. Armentano D, Yu SF, Kantoff PW, von Ruden T, Anderson WF, Gilboa E: Effect of internal viral sequences on the utility of retroviral vectors. J Virol 1987, 61:1647-1650.
56. Bender MA, Palmer TD, Gelinas RE, Miller AD: Evidence that the packaging signal of Moloney murine leukemia virus extends into the gag region. J Virol 1987, 61:1639-1646.
57. Embretson JE, Temin HM: Lack of competition results in efficient packaging of heterologous murine retroviral RNAs and reticuloendotheliosis virus encapsidation-minus RNAs by the reticuloendotheliosis virus helper cell line. J Virol 1987, 61:2675-2683.
58. Knight JB, Si ZH, Stoltzfus CM: A base-paired structure in the avian sarcoma virus 5′ leader is required for efficient encapsidation of RNA. J Virol 1994, 68:4493-4502.
59. Mann R, Baltimore D: Varying the position of a retrovirus packaging sequence results in the encapsidation of both unspliced and spliced RNAs. J Virol 1985, 54:401-407.
60. Sullenger BA, Cech TR: Tethering ribozymes to a retroviral packaging signal for destruction of viral RNA. Science 1993, 262:1566-1569.
61. Watanabe S, Temin HM: 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 1982, 79:5986-5990.
62. Hayashi T, Shioda T, Iwakura Y, Shibuta H: RNA packaging signal of human immunodeficiency virus type 1. Virology 1992, 188:590-599.
63. Kim HJ, Lee K, O'Rear JJ: A short sequence upstream of the 5′ major splice site is important for encapsidation of HIV-1 genomic RNA. Virology 1994, 198:336-340.
64. Dorfman T, Luban J, Goff SP, Haseltine WA, Gottlinger HG: Mapping of functionally important residues of a cysteine-histidine box in the human immunodeficiency virus type 1 nucleocapsid protein. J Virol 1993, 67:6159-6169.
65. Gorelick RJ, Nigida SM Jr, Bess JW Jr, Arthur LO, Henderson LE, Rein A: Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. J Virol 1990, 64:3207-3211.
66. Morellet N, Jullian N, De Rocquigny H, Maigret B, Darlix JL, Roques BP: Determination of the structure of the nucleocapsid protein NCp7 from the human immunodeficiency virus type 1 by 1H NMR. Embo J 1992, 11:3059-3065.
67. Omichinski JG, Clore GM, Sakaguchi K, Appella E, Gronenborn AM: Structural characterization of a 39-residue synthetic peptide containing the two zinc binding domains from the HIV-1 p7 nucleocapsid protein by CD and NMR spectroscopy. FEBS Lett 1991, 292: 25-30.
68. South TL, Summers MF: 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 Psi-site analog, dACGCC. Protein Sci 1993, 2:3-19.
69. Sakaguchi K, Zambrano N, Baldwin ET, Shapiro BA, Erickson JW, Omichinski JG, Clore GM, Gronenborn AM, Appella E: Identification of a binding site for the human immunodeficiency virus type 1 nucleocapsid protein. Proc Natl Acad Sci U S A 1993, 90:5219-5223.
70. Luban J, Goff SP: Mutational analysis of cis-acting packaging signals in human immunodeficiency virus type 1 RNA. J Virol 1994, 68:3784-3793.
71. Dannull J, Surovoy A, Jung G, Moelling K: 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 1994, 13:1525-1533.
72. Berkowitz RD, Luban J, Goff SP: Specific binding of human immunodeficiency virus type 1 gag polyprotein and nucleocapsid protein to viral RNAs detected by RNA mobility shift assays. J Virol 1993, 67:7190-7200.
73. Clever J, Sassetti C, Parslow TG: RNA secondary structure and binding sites for gag gene products in the 5′ packaging signal of human immunodeficiency virus type 1. J Virol 1995, 69: 2101-2109.
74. McBride MS, Panganiban AT: The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J Virol 1996, 70:2963-2973.
75. McBride MS, Panganiban AT: Position dependence of functional hairpins important for human immunodeficiency virus type 1 RNA encapsidation in vivo. J Virol 1997, 71:2050-2058.
76. Zeffman A, Hassard S, Varani G, Lever A: 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 2000, 297:877-893.
77. De Guzman RN, Wu ZR, Stalling CC, Pappalardo L, Borer PN, Summers MF: Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science 1998, 279: 384-388.
78. Amarasinghe GK, De Guzman RN, Turner RB, Chancellor KJ, Wu ZR, Summers MF: 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 2000, 301:491-511.
79. Amarasinghe GK, Zhou J, Miskimon M, Chancellor KJ, McDonald JA, Matthews AG, Miller RR, Rouse MD, Summers MF: Stem-loop SL4 of the HIV-1 psi RNA packaging signal exhibits weak affinity for the nucleocapsid protein. structural studies and implications for genome recognition. J Mol Biol 2001, 314:961-970.
80. Berkowitz RD, Hammarskjold ML, Helga-Maria C, Rekosh D, Goff SP: 5′ regions of HIV-1 RNAs are not sufficient for encapsidation: implications for the HIV-1 packaging signal. Virology 1995, 212:718-723.
81. Helga-Maria C, Hammarskjold ML, Rekosh D: An intact TAR element and cytoplasmic localization are necessary for efficient packaging of human immunodeficiency virus type 1 genomic RNA. J Virol 1999, 73:4127-4135.
82. Kaye JF, Richardson JH, Lever AM: cis-acting sequences involved in human immunodeficiency virus type 1 RNA packaging. J Virol 1995, 69:6588-6592.
83. McBride MS, Schwartz MD, Panganiban AT: Efficient encapsidation of human immunodeficiency virus type 1 vectors and further characterization of cis elements required for encapsidation. J Virol 1997, 71:4544-4554.
84. Parolin C, Dorfman T, Palu G, Gottlinger H, Sodroski J: Analysis in human immunodeficiency virus type 1 vectors of cis-acting sequences that affect gene transfer into human lymphocytes. J Virol 1994, 68:3888-3895.
85. Das AT, Klaver B, Klasens BI, van Wamel JL, Berkhout B: A conserved hairpin motif in the R-U5 region of the human immunodeficiency virus type 1 RNA genome is essential for replication. J Virol 1997, 71:2346-2356.
86. Clever JL, Eckstein DA, Parslow TG: Genetic dissociation of the encapsidation and reverse transcription functions in the 5′ R region of human immunodeficiency virus type 1. J Virol 1999, 73:101-109.
87. Russell RS, Hu J, Laughrea M, Wainberg MA, Liang C: Deficient dimerization of human immunodeficiency virus type 1 RNA caused by mutations of the u5 RNA sequences. Virology 2002, 303: 152-163.
88. Marquet R, Baudin F, Gabus C, Darlix JL, Mougel M, Ehresmann C, Ehresmann B: Dimerization of human immunodeficiency virus (type 1) RNA: stimulation by cations and possible mechanism. Nucleic Acids Res 1991, 19:2349-2357.
89. Bieth E, Gabus C, Darlix JL: A study of the dimer formation of Rous sarcoma virus RNA and of its effect on viral protein synthesis in vitro. Nucleic Acids Res 1990, 18:119-127.
90. Prats AC, Roy C, Wang PA, Erard M, Housset V, Gabus C, Paoletti C, Darlix JL: cis elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J Virol 1990, 64:774-783.
91. Cheung KS, Smith RE, Stone MP, Joklik WK: Comparison of immature (rapid harvest) and mature Rous sarcoma virus particles. Virology 1972, 50:851-864.
92. Korb J, Travnicek M, Riman J: The oncornavirus maturation process: quantitative correlation between morphological changes and conversion of genomic virion RNA. Intervirology 1976, 7: 211-224.
93. Canaani E, Helm KV, Duesberg P: Evidence for 30-40S RNA as precursor of the 60-70S RNA of Rous sarcoma virus. Proc Natl Acad Sci U S A 1973, 70:401-405.
94. Oertle S, Spahr PF: Role of the gag polyprotein precursor in packaging and maturation of Rous sarcoma virus genomic RNA. J Virol 1990, 64:5757-5763.
95. Stewart L, Schatz G, Vogt VM: Properties of avian retrovirus particles defective in viral protease. J Virol 1990, 64:5076-5092.
96. Bowles NE, Damay P, Spahr PF: Effect of rearrangements and duplications of the Cys-His motifs of Rous sarcoma virus nucleocapsid protein. J Virol 1993, 67:623-631.
97. Dupraz P, Oertle S, Meric C, Damay P, Spahr PF: Point mutations in the proximal Cys-His box of Rous sarcoma virus nucleocapsid protein. J Virol 1990, 64:4978-4987.
98. Fu W, Gorelick RJ, Rein A: Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and protease-defective virions. J Virol 1994, 68:5013-5018.
99. Clever JL, Parslow TG: Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation. J Virol 1997, 71:3407-3414.
100. Rong L, Russell RS, Hu J, Laughrea M, Wainberg MA, Liang C: Deletion of stem-loop 3 is compensated by second-site mutations within the Gag protein of human immunodeficiency virus type 1. Virology 2003, 314:221-228.
101. Russell RS, Hu J, Beriault V, Mouland AJ, Laughrea M, Kleiman L, Wainberg MA, Liang C: Sequences downstream of the 5′ splice donor site are required for both packaging and dimerization of human immunodeficiency virus type 1 RNA. J Virol 2003, 77:84-96.
102. Sakuragi J, Shioda T, Panganiban AT: 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 2001, 75:2557-2565.
103. Sakuragi J, Iwamoto A, Shioda T: Dissociation of genome dimerization from packaging functions and virion maturation of human immunodeficiency virus type 1. J Virol 2002, 76:959-967.
104. Russell RS, Roldan A, Detorio M, Hu J, Wainberg MA, Liang C: 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 2003, 77:12986-12995.
105. Shehu-Xhilaga M, Crowe SM, Mak J: Maintenance of the Gag/Gag-Pol ratio is important for human immunodeficiency virus type 1 RNA dimerization and viral infectivity. J Virol 2001, 75: 1834-1841.
106. Laughrea M, Shen N, Jette L, Wainberg MA: Variant effects of non-native kissing-loop hairpin palindromes on HIV replication and HIV RNA dimerization: role of stem-loop B in HIV replication and HIV RNA dimerization. Biochemistry 1999, 38:226-234.
107. Paillart JC, Berthoux L, Ottmann M, Darlix JL, Marquet R, Ehresmann B, Ehresmann C: 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 1996, 70: 8348-8354.
108. Harrison GP, Miele G, Hunter E, Lever AM: Functional analysis of the core human immunodeficiency virus type 1 packaging signal in a permissive cell line. J Virol 1998, 72:5886-5896.
109. Shen N, Jette L, Liang C, Wainberg MA, 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 2000, 74:5729-5735.
110. Sakuragi J, Ueda S, Iwamoto A, Shioda T: Possible role of dimerization in human immunodeficiency virus type 1 genome RNA packaging. J Virol 2003, 77:4060-4069.
111. 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 1997, 36: 9501-9508.
112. Liang C, Rong L, Laughrea M, Kleiman L, Wainberg MA: Compensatory point mutations in the human immunodeficiency virus type 1 Gag region that are distal from deletion mutations in the dimerization initiation site can restore viral replication. J Virol 1998, 72:6629-6636.
113. Liang C, Rong L, Quan Y, Laughrea M, Kleiman L, Wainberg MA: Mutations within four distinct gag proteins are required to restore replication of human immunodeficiency virus type 1 after deletion mutagenesis within the dimerization initiation site. J Virol 1999, 73:7014-7020.
114. Liang C, Rong L, Cherry E, Kleiman L, Laughrea M, Wainberg MA: Deletion mutagenesis within the dimerization initiation site of human immunodeficiency virus type 1 results in delayed processing of the p2 peptide from precursor proteins. J Virol 1999, 73: 6147-6151.
115. Liang C, Rong L, Russell RS, Wainberg MA: Deletion mutagenesis downstream of the 5′ long terminal repeat of human immunodeficiency virus type 1 is compensated for by point mutations in both the U5 region and gag gene. J Virol 2000, 74: 6251-6261.
116. Muriaux D, Mirro J, Harvin D, Rein A: RNA is a structural element in retrovirus particles. Proc Natl Acad Sci U S A 2001, 98:5246-5251.
117. Campbell S, Rein A: In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J Virol 1999, 73:2270-2279.
118. Campbell S, Vogt VM: Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1. J Virol 1995, 69:6487-6497.
119. Ganser BK, Li S, Klishko VY, Finch JT, Sundquist WI: Assembly and analysis of conical models for the HIV-1 core. Science 1999, 283:80-83.
120. Wang SW, Aldovini A: RNA incorporation is critical for retroviral particle integrity after cell membrane assembly of Gag complexes. J Virol 2002, 76:11853-11865.
121. Wang SW, Noonan K, Aldovini A: Nucleocapsid-RNA interactions are essential to structural stability but not to assembly of retroviruses. J Virol 2004, 78:716-723.
122. Sheng N, Pettit SC, Tritch RJ, Ozturk DH, Rayner MM, Swanstrom R, Erickson-Viitanen S: Determinants of the human immunodeficiency virus type 1 p15NC-RNA interaction that affect enhanced cleavage by the viral protease. J Virol 1997, 71: 5723-5732.
123. Skripkin E, Paillart JC, Marquet R, Blumenfeld M, Ehresmann B, Ehresmann C: Mechanisms of inhibition of in vitro dimerization of HIV type 1 RNA by sense and antisense oligonucleotides. J Biol Chem 1996, 271:28812-28817.
124. Ennifar E, Paillart JC, Marquet R, Ehresmann B, Ehresmann C, Dumas P, Walter P: HIV-1 RNA dimerization initiation site is structurally similar to the ribosomal A site and binds aminoglycoside antibiotics. J Biol Chem 2003, 278:2723-2730.
125. Lee NS, Rossi JJ: Control of HIV-1 replication by RNA interference. Virus Res 2004, 102:53-58.
126. Lee NS, Dohjima T, Bauer G, Li H, Li MJ, Ehsani A, Salvaterra P, Rossi J: Expression of small interfering RNAs targeted against HIV-1 rev transcripts in human cells. Nat Biotechnol 2002, 20:500-505.
127. Boden D, Pusch O, Lee F, Tucker L, Ramratnam B: Human immunodeficiency virus type 1 escape from RNA interference. J Virol 2003, 77:11531-11535.
128. Das AT, Brummelkamp TR, Westerhout EM, Vink M, Madiredjo M, Bernards R, Berkhout B: Human immunodeficiency virus type 1 escapes from RNA interference-mediated inhibition. J Virol 2004, 78: 2601-2605.
129. Xie B, Calabro V, Wainberg MA, Frankel AD: Selection of TAR RNA-binding chameleon peptides by using a retroviral replication system. J Virol 2004, 78:1456-1463.
130. Goldschmidt V, Paillart JC, Rigourd M, Ehresmann B, Aubertin AM, Ehresmann C, Marquet R: Structural variability of the initiation complex of HIV-1 reverse transcription. J Biol Chem 2004, 279:35923-35931.
131. Huthoff H, Berkhout B: Multiple secondary structure rearrangements during HIV-1 RNA dimerization. Biochemistry 2002, 41:10439-10445.
132. Abbink TE, Berkhout B: A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the Gag start codon. J Biol Chem 2003, 278:11601-11611.
133. Huthoff H, Berkhout B: Two alternating structures of the HIV-1 leader RNA. RNA 2001, 7:143-157.
134. Knight J: Gene regulation: switched on to RNA. Nature 2003, 425:232-233.
135. Ooms M, Huthoff H, Russell RS, Liang C, Berkhout B: A riboswitch regulates RNA dimerization and packaging in HIV-1 virions. J Virol 2004 in press.
136. Berkhout B, van Wamel JL: The leader of the HIV-1 RNA genome forms a compactly folded tertiary structure. RNA 2000, 6:282-295.