Rev response elements (RRE) in lentiviruses: An RNAMotif algorithm-based strategy for RRE prediction

Medicinal Research Reviews

Volumn 22, Issue 6, 2002, Pages 617-636

  Lesnik, Elena A ^a   Sampath, Ranga ^a   Ecker, David J ^a  

^a Ibis Therapeutics   (United States)

Author keywords

Lentivirus genomes; New computational strategy for prediction of structure and location of putative RREs; Rev responsive elements (RRE)

Indexed keywords

ANTIVIRUS AGENT; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; MESSENGER RNA; REV PROTEIN; RNA; VIRUS ENVELOPE PROTEIN;

ALGORITHM; CAPRINE ARTHRITIS ENCEPHALITIS VIRUS; CELL NUCLEUS; CENTRAL NERVOUS SYSTEM DISEASE; COMPUTER PROGRAM; CYTOPLASM; DNA RESPONSIVE ELEMENT; FELINE IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; IMMUNOPATHOLOGY; LENTIVIRINAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA SPLICING; RNA STRUCTURE; RNA TRANSPORT; SIMIAN IMMUNODEFICIENCY VIRUS; THERMODYNAMICS; VIRUS GENOME; VISNA VIRUS;

ALGORITHMS; ANIMALS; COMPUTATIONAL BIOLOGY; GENE PRODUCTS, REV; HIV-1; HIV-2; HUMANS; LENTIVIRUS; PRIMATES; RESPONSE ELEMENTS; THERMODYNAMICS;

EID: 0036846922     PISSN: 01986325     EISSN: None     Source Type: Journal    
DOI: 10.1002/med.10027     Document Type: Review

References (105)

1. Henkin TM. Control of transcription termination in prokaryotes. Annu Rev Genet 1996;30:35-57.
2. Cullen BR. Mechanism of action of regulatory proteins encoded by complex retroviruses. Microbiol Rev 1992;56:375-394.
3. Theil EC. The iron responsive element (IRE) family of mRNA regulators; regulation of iron transport and uptake compared in animals, plants, and microorganisms. Met Ions Biol Syst 1998;35:403-434.
4. Tang H, Kuhen KL, Wong-Staal F. Lentivirus replication and regulation. Annu Rev Genet 1999;33:133-170.
5. Macke T, Ecker DJ, Gutell R, Gautheret D, Case D, Sampath R. RNA motif - An RNA secondary structure definition and search algorithm. Nuc Acids Res 2001;29:4724-4735.
6. Lesnik EA, Sampath R, Levene HB, Henderson TJ, McNeil JA, Ecker DJ. Prediction of rho-independent transcriptional terminators in Escherichia coli. Nucleic Acids Res 2001;29:3583-3594.
7. Mathews DH, Sabina J, Zuker M, Turner DH. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 1999;288:911-940.
8. Battiste JL, Mao H, Rao NS, Ran R, Muhandiram DR, Kay LE, Frankel AD, Williamson JR. α helix-RNA major groove recognition in an HIV-1 Rev peptide-RRE RNA complex. Science 1996;273:1547-1551.
9. Ye X, Gorin A, Ellington AD, Patel DJ. Deep penetration of an alpha-helix into a widened RNA major groove in the HIV-1 rev peptide-RNA aptamer complex. Nature Struct Biol 1996;3:1026-1033.
10. Battiste JL, Tan R, Frankel AD, Williamson JR. Binding of an HIV rev peptide to rev responsive element RNA induces formation of purine-purine base pairs. Biochemistry 1994;33:2741-2747.
11. Peterson RD, Feigon J. Structural change in Rev responsive element RNA of HIV-1 on binding Rev peptide. J Mol Biol 1996;264:863-877.
12. Wilkinson TA, Botuyan MV, Kaplan BE, Rossi JJ, Chen Y. Arginine side-chain dynamics in the HIV-1 rev-RRE complex. J Mol Biol 2000;303:515-529.
13. Gosser Y, Hermann T, Majumdar A, Hu W, Frederick R, Jiang F, Xu W, Patel DJ. Peptide-triggered conformational switch in HIV-1 RRE RNA complexes. Nat Struct Biol 2001;8:146-150.
14. Charpentier B, Stutz F, Rosbash M. A dynamic in vivo view 6f the HIV-1 Rev-RRE interaction. J Mol Biol 1997;266:950-962.
15. Peterson RD, Bartel DP, Szostak JW, Horvath SJ, Feigon J. 1H NMR studies of the high-affinity Rev binding site of the Rev responsive element of HIV-1 mRNA: base pairing in the core binding element. Biochemistry 1994;33:5357-5366.
16. Hung LW, Holbrook EL, Holbrook SR. The crystal structure of the rev binding element of HIV-1 reveals novel base pairing and conformational variability [In Process Citation]. Proc Natl Acad Sci USA 2000;97:5107-5112.
17. Felber BK. Regulation of mRNA expression in HIV-1 and other retroviruses. Mod Cell Biol 1997;17:323-340.
18. Felber BK. Posttranscriptional control: a general and important regulatory feature of HIV-1 and other retroviruses In: Myers G, Myers G, editors Viral Regulatory Structures. Los Alamos, NM: Addison-Wesley; 1998. p. 101-122.
19. Cullen BR. Retroviruses as model systems for the study of nuclear RNA export pathways. Virol 1998;249:203-210.
20. Kjems J, Askjaer P. Rev protein and its cellular partners. Adv Pharmacol 2000;48:251-98.
21. Izaurralde E, Adam S. Transport of macromolecules between the nucleus and the cytoplasm. RNA 1998;4:351-364.
22. Nakielny S, Dreyfuss G. Nuclear export of proteins and RNAs. Curr Opin Cell Biol 1997;9:420-429.
23. Malim MH, Hauber J, Le S-Y, Maizel JV, Cullen BR. The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 1989;338:254-257.
24. Rosen CA, Terwilliger E, Dayton A, Sodroski JG, Haseltine WA. Intragenic cis-acting art gene-responsive sequences of the human immunodeficiency virus. Proc Natl Acad Sci USA 1988;85:2071-2075.
25. Dayton ET, Powell DM, Dayton AI. Functional analysis of CAR, the target sequence for the Rev protein of HIV-1. Science 1989;246:1625-1629.
26. Malim MH, Bohnlein S, Fenrick R, Le SY, Maizel JV, Cullen BR. Functional comparison of the Rev transactivators encoded by different primate immunodeficiency virus species. Proc Natl Acad Sci USA 1989;86:8222-8226.
27. Mann DA, Mikaelian I, Zemmel RW, Green SM, Lowe AD, Kimura T, Singh M, Butler PJG, Gait MJ, Karn J. A molecular rheostat. Co-operative rev binding to stem I of the rev-response element modulates human immunodeficiency virus type-1 late gene expression. J Mol Biol 1994;241:193-207.
28. Zhang MJ, Dayton AI. Two secondary structures for the RRE of HIV-1? J Acquir Immune Defic Syndr Hum Retrovirol 1996;13:403-407.
29. Hope TJ. The ins and outs of HIV Rev. Arch Biochem Biophys 1999;365:186-191.
30. Pollard VW, Malim MH. The HIV-1 Rev protein. Annu Rev Microbiol 1998;52:491-532.
31. Le SY, Malim MH, Cullen BR, Maizel JV. A highly conserved RNA folding region coincident with the Rev response element of primate immunodeficiency viruses. Nucleic Acids Res 1990;18:1613-1623.
32. Malim MH, Tiley LS, McCarn DF, Rusche JR, Hauber J, Cullen BR. HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence. Cell 1990;60:675-683.
33. Kjems J, Brown M, Chang DD, Sharp PA. Structural analysis of the interaction between the human immunodeficiency virus Rev protein and the Rev response element. Proc Natl Acad Sci USA 1991;88:683-687.
34. Dillon PJ, Nelbock P, Perkins A, Rosen CA. Function of the human immunodeficiency virus types 1 and 2 Rev proteins is dependent on their ability to interact with a structured region present in env gene mRNA. J Virol 1990;64:4428-4437.
35. Patel DJ. Adaptive recognition in RNA complexes with peptides and protein modules. Curr Opin Struct Biol 1999;9:74-87.
36. Draper DE. Themes in RNA-protein recognition. Journal Molecular Biology 1999;293:255-270.
37. Malim MH, Tiley LS, McCarn DF, Rusche JR, Hauber J, Cullen BR. HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence. Cell 1990;60:675-683.
38. Bartel DP, Zapp ML, Green MR, Szostak JW. HIV-1 Rev Regulation involves recognition of Non-Watson-Crick base pairs in viral RNA. Cell 1991;67:529-536.
39. Heaphy S, Dingwall C, Ernberg I, Gait MJ, Green SM, Karn J, Lowe AD, Singh M, Skinner MA. HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region. Cell 1990;60:685-693.
40. Kjems J, Calnan BJ, Frankel AD, Sharp PA. Specific binding of a basic peptide from HIV-1 Rev. EMBO J 1992;11:1119-1129.
41. Tiley LS, Malim MH, Tewary HK, Stockley PG, Cullen BR. Identification of a high-affinity RNA-binding site for the human immunodeficiency virus type 1 Rev protein. Proc Natl Acad Sci USA 1992;89:758-762.
42. Iwai S, Pritchard C, Mann DA, Karn J, Gait MJ. Recognition of the high affinity binding site in rev-response element RNA by the human immunodeficiency virus type-1 rev protein. Nucl Acids Res 1992;20:6465-6472.
43. Grate D, Wilson C. Role REVersal: Understanding how RRE RNA binds its peptide ligand. Structure 1997;5:7-11.
44. Cole JL, Gehman JD, Shafer JA, Kuo LC. Solution oligomerization of the rev protein of HIV-1: Implications for function. Biochemistry 1993;32:11769-11775.
45. Daly TJ, Doten RC, Rennert P, Auer M, Jaksche H, Donner A, Fisk G, Rusche JR. Biochemical characterization of binding of multiple HIV-1 Rev monomeric proteins to the Rev responsive element. Biochemistry 1993;32:10497-10505.
46. Madore SJ, Tiley LS, Malim MH, Cullen BR. Sequence requirements for Rev multimerization in vivo. Virol 1994;202:186-194.
47. Malim MH, Cullen BR. HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: Implications for HIV-1 latency. Cell 1991;65:241-248.
48. Jain C, Belasco JG. Structural model for the cooperative assembly of HIV-1 Rev multimers on the RRE as deduced from analysis of assembly-defective mutants. Mol Cell 2001;7:603-614.
49. Van Ryk DI, Venkatesan S. Real-time kinetics of HIV-1 Rev-Rev response element interactions. Definition of minimal binding sites on RNA and protein and stoichiometric analysis. J Biol Chem 1999;274:17452-17463.
50. Zapp ML, Hope TJ, Parslow TG, Green MR. Oligomerization and RNA binding domains of the type 1 human immunodeficiency virus Rev protein: A dual function for an arginine-rich binding motif. Proc Natl Acad Sci USA 1991;88:7734-7738.
51. Holland SM, Ahmad N, Maitra RK, Wingfield P, Venkatesan S. Human immunodeficiency virus Rev protein recognizes a target sequence in Rev-responsive element RNAwithin the context of RNA secondary structure. J Virol 1990;64:5966-5975.
52. Thomas SL, Oft M, Jaksche H, Casari G, Heger P, Dobrovnik M, Bevec D, Hauber J. Functional analysis of the human immunodeficiency virus type 1 Rev protein oligomerization interface. J Virol 1998;72:2935-2944.
53. Daly TJ, Cook KS, Gray GS, Maione TE, Rusche JR. Specific binding of HIV-1 recombinant Rev protein to the Rev-responsive element in vitro. Nature 1989;342:816-819.
54. Karn J, Dingwall C, Finch JT, Heaphy S, Gait MJ. RNA binding by the tat and rev proteins of HIV-1. Biochimie 1991;73:9-16.
55. Nalin CM, Purcell RD, Antelman D, Mueller D, Tomchak L, Wegrzynski B, McCarney E, Toome V, Kramer R, Hsu M-C. Purification and characterization of recombinant Rev protein of human immunodeficiency virus type 1. Proc Natl Acad Sci USA 1990;87:7593-7597.
56. Wingfield PT, Stahl SJ, Payton MA, Venkatesan S, Misra M, Steven AC. HIV-1 Rev expressed in recombinant Escherichia coli: Purification, polymerization, and conformational properties. Biochemistry 1991;30:7527-7534.
57. Zapp ML, Green MR. Sequence-specific RNA binding by the HIV-1 Rev protein. Nature 1989;343:714-716.
58. Bogerd H, Greene WC. Dominant negative mutants of human T-cell leukemia virus type I Rex and human immunodeficiency virus type 1 Rev fail to multimerize in vivo. J Virol 1993;67:2496-2502.
59. Hope TJ, Klein NP, Elder ME, Parslow TG. Trans-dominant inhibition of human immunodeficiency virus type 1 Rev occurs through formation of inactive protein complexes. J Virol 1992;66:1849-1855.
60. Kubota S, Furuta R, Maki M, Hatanaka M. Inhibition of human immunodeficiency virus type 1 Rev function by a Rev mutant which interferes with nuclear/nucleolar localization of Rev J Virol 1992;66:2510-2513.
61. Olsen HS, Cochrane AW, Dillon PJ, Nalin CM, Rosen CA. Interaction of the human immunodeficiency virus type 1 Rev protein with a structured region in env mRNA is dependent on multimer formation mediated through a basic stretch of amino acids. Genes Dev 1990;4:1357-1364.
62. Stauber R, Gaitanaris GA, Pavlakis GN. Analysis of trafficking of Rev and transdominant Rev proteins in living cells using green fluorescent protein fusions: Transdominant Rev blocks the export of Rev from the nucleus to the cytoplasm. Virol 1995;213:439-449.
63. Zemmel RW, Kelley AC, Karn J, Butler PJG. Flexible regions of RNA structure facilitate co-operative Rev assembly on the Rev-response element. Journal of Molecular Biology 1996;258:763-777.
64. McClure MA. The complexities of viral genome analysis: The primate lentiviruses. Curr Opin Genet Dev 1996;6:749-756.
65. Lewis N, Williams J, Rekosh D, Hammarskjold ML. Identification of a cis-acting element in human immunodeficiency virus type 2 (HIV-2) that is responsive to the HIV-1 rev and human T-cell leukemia virus types I and II rex proteins. J Virol 1990;64:1690-1697.
66. Garrett ED, Cullen BR. Comparative analysis of Rev function in human immunodeficiency virus types 1 and 2. J Virol 1992;66:4288-4294.
67. Guyader M, Emerman M, Sonigo P, Clavel F, Montagnier L, Alizon M. Genome organization and transactivation of the human immunodeficiency virus type 2. Nature 1987;326:662-669.
68. Chen JH, Le SY, Maizel JV. Prediction of common secondary structures of RNAs: A genetic algorithm approach. Nucleic Acids Res 2000;28:991-999.
69. Kuiken CL, Foley B, Hahn B, Marx P, McCutchan F, Mellors JW, Mullins J, Wolinsky S, Korber B. Human Retroviruses and AIDS 1999: A Compilation of Nucleic Acid and Amino Acid Sequences. Los Alamos, NM: Theoretical Biology and Biophysics Group, Los Alamos Natl Lab; 1999. p. iv.
70. Pepin M, Vitu C, Russo P, Mornex JF, Peterhans E. Maedi-visna virus infection in sheep: A review. Vet Res 1998;29:341-367.
71. Gonda MA, Wong-Staal F, Gallo RC, Clements JE, Narayan O, Gilden RV. Sequence homology and morphologic similarity of HTLV-III and visna virus, a pathogenic lentivirus. Science 1985;227:173-177.
72. Tiley LS, Brown PH, Le SY, Maizel JV, Clements JE, Cullen BR. Visna virus encodes a post-transcriptional regulator of viral structural gene expression. Proc Natl Acad Sci USA 1990;87:7497-7501.
73. Sonigo P, Alizon M, Staskus K, Klatzmann D, Cole S, Danos O, Retzel E, Tiollais P, Haase A, Wain-Hobson S. Nucleotide sequence of the visna lentivirus: Relationship to the AIDS virus. Cell 1985;42:369-382.
74. Tiley LS, Cullen BR. Structural and functional analysis of the Visna virus Rev-responsive element. J Virology 1992;66:3609-3615.
75. Cork LC, Hadlow WJ, Gorham JR, Piper RC, Crawford TB. Pathology of viral leukoencephalomyelitis of goats. Acta Neuropathol 1974;29:281-292.
76. Saltarelli MJ, Schoborg R, Pavlakis GN, Clements JE. Identification of the caprine arthritis encephalitis virus Rev protein and its cis-acting Rev-responsive element. Virol 1994;199:47-55.
77. Schoborg RV, Clements JE. Definition of the RRE binding and activation domains of the caprine arthritis encephalitis virus Rev protein. Virol 1996;226:113-121.
78. Saltarelli M, Querat G, Konings DAM, Vigne R, Clements JE. Nucleotide sequence and transcriptional analysis of molecular clones of CAEV which generate infectious virus. Virol 1990;179:347-364.
79. Querat G, Barban V, Sauze N, Vigne R, Payne A, York D, De Villiers EM, Verwoerd DW. Characteristics of a novel lentivirus derived from South African sheep with pulmonary adenocarcinoma (jaagsiekte). Virol 1987;158:158-167.
80. Mwaengo DM, Grant RF, DeMartini JC, Carlson JO. Envelope glycoprotein nucleotide sequence and genetic characterization of North American ovine lentiviruses. Virol 1997;238:135-144.
81. Miyazawa T, Tomonaga K, Kawaguchi Y, Mikami T. The genome of feline immunodeficiency virus. Arch Virol 1994;134:221-234.
82. Bendinelli M, Pistello M, Lombardi S, Poli A, Garzelli C, Matteucci D, Ceccherini-Nelli L, Malvaldi G, Tozzini F. Feline immunodeficiency virus: An interesting model for AIDS studies and an important cat pathogen. Clinical Microbiology Reviews 1995;8:87-112.
83. Kiyomasu T, Miyazawa T, Furuya T, Shibata R, Sakai H, Sakuragi J, Fukasawa M, Maki N, Hasegawa A, Mikami T, et al. Identification of feline immunodeficiency virus rev gene activity. J Virol 1991;65:4539-4542.
84. Talbott RL, Sparger EE, Lovelace KM, Fitch WM, Pedersen NC, Luciw PA, Elder JH. Nucleotide sequence and genomic organization of feline immunodeficiency virus. Proc Natl Acad Sci USA 1989;86:5743-5747.
85. Olmsted RA, Hirsch VM, Purcell RH, Johnson PR. Nucleotide sequence analysis of feline immunodeficiency virus: Genome organization and relationship to other lentiviruses. Proc Natl Acad Sci USA 1989;86:8088-8092.
86. Phillips TR, Lamont C, Konings DA, Shacklett BL, Hamson CA, Luciw PA, Elder JH. Identification of the Rev transactivation and Rev-responsive elements of feline immunodeficiency virus. J Virol 1992;66:5464-5471.
87. Zou L, Barr MC, Hoose WA, Avery RJ. Characterization of the transcription map and Rev activity of a highly cytopathic feline immunodeficiency virus. Virol 1997;236:266-278.
88. Mergia A, Blackwell J, Chari S. Inhibition of FIV replication by a ribozyme that targets the Rev response element. AIDS ResHumRetroviruses 1997;13:1333-1339.
89. Belshan M, Harris ME, Shoemaker AE, Hope TJ, Carpenter S. Biological characterization of Rev variation in equine infectious anemia virus. J Virol 1998;72:4421-4426.
90. Harris ME, Gontarek RR, Derse D, Hope TJ. Differential requirements for alternative splicing and nuclear export functions of equine infectious anemia virus Rev protein. Mol Cell Biol 1998;18:3889-3899.
91. Fridell RA, Partin KM, Carpenter S, Cullen BR. Identification of the activation domain of equine infectious anemia virus rev. J Virol 1993;67:7317-7323.
92. Mancuso VA, Hope TJ, Zhu L, Derse D, Phillips T, Parslow TG. Posttranscriptional effector domains in the Rev proteins of feline immunodeficiency virus and equine infectious anemia virus. J Virol 1994;68:1998-2001.
93. Martarano L, Stephens R, Rice N, Derse D. Equine infectious anemia virus trans-regulatory protein Rev controls viral mRNA stability, accumulation, and alternative splicing. J Virol 1994;68:3102-3111.
94. Chung H, Derse D. Binding sites for Rev and ASF/SF2 map to a 55-nucleotide purine-rich exonic element in equine infectious anemia virus RNA. J Biol Chem 2001;276:18960-18967.
95. Gontarek RR, Derse D. Interactions among SR proteins, an exonic splicing enhancer, and a lentivirus Rev protein regulate alternative splicing. Mol Cell Biol 1996;16:2325-2331.
96. Belshan M, Park GS, Bilodeau P, Stoltzfus CM, Carpenter S. Binding of equine infectious anemia virus rev to an exon splicing enhancer mediates alternative splicing and nuclear export of viral mRNAs. Mol Cell Biol 2000;20:3550-3557.
97. Chadwick BJ, Coelen RJ, Wilcox GE, Sammels LM, Kertayadnya G. Nucleotide sequence analysis of Jembrana disease virus: A bovine lentivirus associated with an acute disease syndrome. J Gen Virol 1995;76:1637-1650.
98. Oberste MS, Williamson JC, Greenwood JD, Nagashima K, Copeland TD, Gonda MA. Characterization of bovine immunodeficiency virus rev cDNAs and identification and subcellular localization of the Rev protein. J Virol 1993;67:6395-405.
99. Garvey KJ, Oberste MS, Elser JE, Braun MJ, Gonda MA. Nucleotide sequence and genome organization of biologically active proviruses of the bovine immunodeficiency-like virus. Virol 1990;175:391-409.
100. Kuiken CL, Foley B, Hahn B, Marx P, McCutchan F, Mellors JW, Mullins J, Wolinsky S, Korber B. Human Retroviruses and AIDS 1999: A Compilation of Nucleic Acid and Amino Acid Sequences. Los Alamos, NM: Theoretical Biology and Biophysics Group, Los Alamos Natl Lab; 1999. p. 789.
101. Bogerd HP, Tiley LS, Cullen BR. Specific binding of the human T-cell leukemia virus type I Rex protein to a short RNA sequence located within the Rex-response element. J Virol 1992;66:7572-7575.
102. Ahmed YF, Hanly SM, Malim MH, Cullen BR, Greene WC. Structure-function analyses of the HTLV-1 Rex and HIV-1 Rev RNA response elements: Insights into the mechanisms of Rex and Rev action. Genes Develop 1990;4:1014-1022.
103. Baskerville S, Zapp M, Ellington AD. High-resolution mapping of the human T-cell leukemia virus type 1 Rex-binding element by in vitro selection. J Virol 1995;69:7559-7569.
104. Foley BT. An overview of the molecular phylogeny of lentiviruses In: Kuiken C, McCutchan F, Foley B, Mellors JW, Hahn B, Mullins J, Marx P, Wolinsky S, Kuiken C, McCutchan F, Foley B, Mellors JW, Hahn B, Mullins J, Marx P, Wolinsky S, editors. HIV Sequence Compendium 2000. Los Alamos: Theoretical Biology and Biophysics Group, Los Alamos Nat Lab; 2000. p. 35-43.
105. Bogerd HP, Fridell RA, Benson RE, Hua J, Cullen BR. Protein sequence requirements for function of the human T-cell leukemia virus type 1 Rex nuclear export signal delineated by a novel in vivo randomization-selection assay. Mol Cell Biol 1996;16:4207-4214.