RNA conformational changes in the life cycles of RNA viruses, viroids, and virus-associated RNAs

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1789, Issue 9-10, 2009, Pages 571-583

  Simon, Anne E ^a   Gehrke, Lee ^b  

^a Bldg 142   (United States)

^b HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

RNA processing; RNA pseudoknot; RNA structural switch; RNA structure; RNA virus replication; RNA protein interaction

Indexed keywords

ADENOSINE PHOSPHATE; CASPASE; HEPATITIS DELTA ANTIGEN; RNA DIRECTED RNA POLYMERASE; RNA HELICASE; VIRUS RNA;

3' UNTRANSLATED REGION; ALFALFA MOSAIC VIRUS; ARTERIVIRUS; CONFORMATIONAL TRANSITION; CORONAVIRUS; CYCLIZATION; ENZYME ACTIVATION; FLAVIVIRUS; HEPATITIS DELTA VIRUS; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; REVIEW; RIBOSWITCH; RNA BINDING; RNA CONFORMATION; RNA PROCESSING; RNA REPLICATION; RNA STRUCTURE; RNA TRANSCRIPTION; RNA TRANSLATION; RNA VIRUS; TURNIP CRINKLE VIRUS; VIROID; VIRUS ASSOCIATED RNA; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ANIMALS; BASE SEQUENCE; CATALYSIS; GENOME, VIRAL; HEPATITIS DELTA VIRUS; HUMANS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA; RNA VIRUSES; RNA, VIRAL; THERMODYNAMICS; TIME FACTORS; VIROIDS;

RNA VIRUSES; VIROIDS;

EID: 71849084955     PISSN: 18749399     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2009.05.005     Document Type: Review

References (148)

1. Chu V.B., and Herschlag D. Unwinding RNA's secrets: advances in the biology, physics, and modeling of complex RNAs. Curr. Opin. Struct. Biol. 18 (2008) 305-314
2. Hermann T., and Patel D.J. Stitching together RNA tertiary architectures. J. Mol. Biol. 294 (1999) 829-849
3. Tinocco Jr. I., and Bustamante C. How RNA folds. J. Mol. Biol. 293 (1999) 271-281
4. Hendrix D.K., Brenner S.E., and Holbrook S.R. RNA structural motifs: building blocks of a modular biomolecule. Quart. Rev. Biophysics 38 (2005) 221-243
5. Al-Hashimi H.M., and Walter N.G. RNA dynamics: it is about time. Curr. Opin. Struct. Biol. 18 (2008) 321-329
6. Edwards T.E., Klein D.J., and Ferré-D Amaré A.R. Riboswitches: small-molecule recognition by gene regulatory RNAs. Curr. Opin. Struct. Biol. 17 (2007) 273-279
7. Henkins T.M. Riboswitch RNAs: using RNA to sense cellular metabolism. Genes Dev. 22 (2008) 3383-3390
8. Serganov A., and Patel D.J. Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nature Rev. 8 (2007) 776-790
9. Bobobza S., Adato A., Mandel T., Shapira M., Nudler E., and Aharoni A. Riboswitch-dependent gene regulation and its evolution in the plant kingdom. Genes Dev. 21 (2007) 2874-2879
10. Ray P.S., Jia J., Yao P., Majumder M., Hatzoglou M., and Fox P.L. A stress-responsive RNA switch regulates VEGFA expression. Nature 457 (2009) 915-920
11. Sudarsan N., Barrick J.E., and Breaker R.R. Metabolite-binding RNA domains are present in the genes of eukaryotes. RNA 9 (2003) 644-647
12. Wachter A., Tunc-Ozdemir M., Grove B.C., Green P.J., Shintani D.K., and Breaker R.R. Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mRNAs. Plant Cell 19 (2007) 3437-3450
13. Ahlquist P. Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nature Rev. Microbiol. 4 (2006) 371-382
14. Buck K.W. Comparison of the replication of positive-stranded RNA viruses of plants and animals. Adv. Virus Res. 47 (1996) 159-251
15. Kopek B.G., Perkins G., Miller D.J., Ellisman M.H., and Ahlquist P. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 5 (2007) 2022-2034
16. Chao L., Rang C.U., and Wong L.E. Distribution of spontaneous mutants and inferences about the replication mode of the RNA bacteriophage φ{symbol}6. J. Virol. 76 (2002) 3276-3281
17. Leontis N.B., Stombaugh J., and Westhof E. The non-Watson-Crick base pairs and their associated isostericity matrices. Nucleic. Acids Res. 30 (2002) 3497-3531
18. J. Stombaugh, C.L. Zirbel, E. Westhof, N.B. Leontis, Frequency and isostericity of RNA base pairs, Nucleic Acids Res. 37 (2009) 2294-2312.
19. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic. Acids Res. 31 (2003) 3406-3415
20. Shapiro B.A., Yingling Y.G., Kasprzak W., and Bindewald E. Bridging the gap in RNA structure prediction. Curr. Opin. Struct. Biol. 17 (2007) 157-165
21. Pan T., and Sosnick T. RNA folding during transcription. Annu. Rev. Biomol. Struct. 35 (2006) 161-175
22. Vilfan I.D., Candelli A., Hage S., Aalto A.P., Poranen M.M., Bamford D.H., and Dekker N.H. Reinitiated viral RNA-dependent RNA polymerase resumes replication at a reduced rate. Nucleic. Acids Res. 36 (2008) 7059-7067
23. Herschlag D. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270 (1995) 20871-20874
24. Landick R. The regulatory roles and mechanism of transcriptional pausing. Biochem. Soc. Trans. 34 (2006) 1062-1066
25. Shapiro B.A., Kasprzak W., Grunewald C., and Aman J. Graphical exploratory data analysis of RNA secondary structure dynamics predicted by the massively parallel genetic algorithm. J. Mol. Graph. Model. 25 (2006) 514-531
26. Ding B., and Itaya A. Viroids: a useful model for studying the basic principles of infection and RNA biology. Mol. Plant Microbe Interact. 20 (2007) 7-20
27. Gas M.-E., Molina-Serrano D., Hernandez C., Flores R., and Daros J.A. Monomeric linear RNA of Citrus exocortis viroid resulting from processing in vivo has 5′ phosphomonoester and 3′ hydroxyl termini: implications for the RNase and RNA ligase involved in replication. J. Virol. 82 (2008) 10321-10325
28. Baumstark T., Schröder A.R.W., and Riesner D. Viroid processing: switch from cleavage to ligation is driven by a change from a tetraloop to a loop E conformation. EMBO J. 16 (1997) 599-610
29. Baumstark T., and Riesner D. Only one of four possible secondary structures of the central conserved region of Potato spindle tuber viroid is a substrate for processing in a potato nuclear extract. Nucleic. Acids Res. 23 (1995) 4246-4254
30. Schröder A.R.W., Baumstark T., and Riesner D. Chemical mapping of co-existing RNA structures. Nucleic. Acids Res. 26 (1998) 3449-3450
31. Schrader O., Baumstark T., and Riesner D. A mini-RNA containing the tetraloop, wobble-pair and loop E motifs of the central conserved region of Potato spindle tuber viroid is processed into a minicircle. Nucleic. Acids Res. 31 (2003) 988-998
32. Gas M.E., Hernandez C., Flores R., and Daros J.A. Processing of nuclear viroids in vivo: an interplay between RNA conformations. PLoS Path. 3 (2007) 1813-1826
33. Diener T.O. Viroid processing: a model involving the central conserved region and hairpin I. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 58-62
34. Shapiro B.A., Bengali D., Kasprzak W., and Wu J.C. RNA folding pathway functional intermediates: their prediction and analysis. J. Mol. Biol. 312 (2001) 27-44
35. Shapiro B.A., and Kasprzak W. STRUCTURELAB: a heterogeneous bioinformatics system for RNA structure analysis. J. Mol. Graph. 14 (1996) 194-205
36. Gross H.J., Domdey H., Lossow C.H., Jank P., Raba M., Alberty H., and Sanger H.L. Nucleotide sequence and secondary structure of Potato spindle tuber viroid. Nature 273 (1978) 203-208
37. Schröder A.R.W., and Riesner D. Detection and analysis of hairpin II, an essential metastable structural element in viroid replication intermediates. Nucleic Acids Res. 30 (2002) 3349-3359
38. Rizzetto M. The delta agent. Hepatology 3 (1983) 729-737
39. Ke A., Zhou K., Ding F., Cate J.H.D., and Doudna J.A. A conformational switch controls hepatitis delta virus ribozyme catalysis. Nature 429 (2004) 201-205
40. Lai M.M.C. The molecular biology of hepatitis delta virus. Annu. Rev. Biochem. 64 (1995) 259-286
41. Perrotta A.T., and Been M.D. A pseudoknot-like structure required for efficient self-cleavage of hepatitis delta virus RNA. Nature 350 (1991) 434-436
42. Wang K.S., Choo Q.L., Ou A.J., Weiner J.H., Najarian R.C., Thayer R.M., Mullenbach G.T., Denniston K.J., Gerin J.L., and Houghton M. Structure, sequence and expression of the hepatitis delta viral genome. Nature 323 (1986) 508-514
43. Doudna J.A., and Lorsch J.R. Ribozyme catalysis: not different, just worse. Nature Struct. Mol. Biol. 12 (2005) 395-402
44. Strobel S.A., and Cochrane J.C. RNA catalysis: Ribozymes, ribosomes and riboswitches. Curr. Opin. Chem. Biol. 11 (2007) 636-643
45. Luo G.T., Chao M., Hsieh S.Y., Sureau C., Nishikura K., and Taylor J. A specific base transition occurs on replicating hepatitis delta virus RNA. J. Virol. 64 (1990) 1021-1027
46. Xia Y.P., Chang M.F., Wei D., Govindarajan S., and Lai M.M. Heterogeneity of hepatitis delta antigen. Virology 178 (1990) 331-336
47. Casey J.L. RNA editing in hepatitis delta virus. Curr. Top. Microbiol. Immunol. 307 (2006) 67-89
48. Casey J.L., Bergmann K.F., Brown T.L., and Gerin J.L. Structural requirements for RNA editing in hepatitis delta virus: evidence for a uridine-to-cytidine editing mechanism. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 7149-7153
49. Wong S.K., and Lazinski D.W. Replicating hepatitis delta virus RNA is edited in the nucleus by the small form of ADAR1. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 15118-15123
50. Casey J.L. RNA editing in hepatitis delta virus genotype III requires a branched double-hairpin RNA structure. J. Virol. 76 (2002) 7385-7397
51. Wong S.K., Sato S., and Lazinski D.W. Substrate recognition by ADAR1 and ADAR2. RNA 7 (2001) 846-858
52. Linnstaedt S.D., Kasprzak W.K., Shapiro B.A., and Casey J.L. The role of a metastable RNA secondary structure in hepatitis delta virus genotype III RNA editing. RNA 12 (2006) 1521-1533
53. Sato S., Cornillez-Ty C., and Lazinski D.W. By inhibiting replication, the large hepatitis delta antigen can indirectly regulate amber/W editing and its own expression. J. Virol. 78 (2004) 8120-8134
54. Jayan G.C., and Casey J.L. Effects of conserved RNA secondary structures on hepatitis delta virus genotype I NRA editing, replication, and virus production. J. Virol. 79 (2005) 11187-11193
55. Cheng Q., Jayan G.C., and Casey J.L. Differential inhibition of RNA editing in hepatitis delta virus genotype III by the short and long forms of hepatitis delta antigen. J. Virol. 77 (2003) 7786-7795
56. S.D. Linnstaedt, W.K. Kasprzak, B.A. Shapiro, J.L. Casey, The fraction of RNA that folds into the correct branched secondary structure determines hepatitis delta virus type 3 RNA editing levels, RNA 15 (2009) 1177-1187.
57. González J.M., Gomez-Puertas P., Cavanagh D., Gorbalenya A.E., and Enjuanes L. A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch. Virol. 8 (2003) 2207-2235
58. Lai M.M.C., and Cavanagh D. The molecular biology of coronaviruses. Adv. Virus Res. 48 (1997) 1-100
59. Masters P.S. The molecular biology of coronaviruses. Adv. Virus. Res. 66 (2006) 193-292
60. Masters P.S. Genomic cis-acting elements in coronavirus RNA replication. In: Thiel V. (Ed). Coronaviruses: Molecular and Cellular Biology (2007), Caister Academic Press, Norwich, United Kingdom 63-78
61. Williams G.D., Chang R.Y., and Brian D.A. A phylogenetically conserved hairpin-type 3′ untranslated region pseudoknot functions in coronavirus RNA replication. J. Virol. 73 (1999) 8349-8355
62. Hsue B., and Masters P.S. A bulged stem-loop structure in the 3′ untranslated region of the genome of the coronavirus mouse hepatitis virus is essential for replication. J. Virol. 71 (1997) 7567-7578
63. Hsue B., Hartshorne T., and Masters P.S. Characterization of an essential RNA secondary structure in the 3′ untranslated region of the murine coronavirus genome. J. Virol. 74 (2000) 6911-6921
64. Goebel S.J., Taylor J., and Masters P.S. The 3′ cis-acting genomic replication element of the severe acute respiratory syndrome coronavirus can function in the murine coronavirus genome. J. Virol. 78 (2004) 7846-7851
65. Goebel S.J., Hsue B., Dombrowski T.F., and Masters P.S. Characterization of the RNA components of a putative molecular switch in the 3′ untranslated region of the murine coronavirus genome. J. Virol. 78 (2004) 669-682
66. Zust R., Miller T.B., Goebel S.J., Thiel V., and Masters P.S. Genetic interactions between an essential 3′ cis-acting RNA pseudoknot replicase gene products, and the extreme 3′ end of the mouse coronavirus genome. J. Virol. 82 (2008) 1214-1228
67. Lin Y.-J., Liao C.-L., and Lai M.M.C. Identification of the cis-acting signal for minus-strand RNA synthesis of a murine coronavirus: implications for the role of minus-strand RNA in RNA replication and transcription. J. Virol. 68 (1994) 8131-8140
68. Beerens N., and Snijder E.J. RNA signals in the 3′ terminus of the genome of Equine arteritis virus are required for viral RNA synthesis. J. Gen Virol. 87 (2006) 1977-1983
69. Beerens N., and Snijder E.J. An RNA pseudoknot in the 3′ end of the Arterivirus genome has a critical role in regulating viral RNA synthesis. J. Virol. 81 (2007) 9426-9436
70. Simon A.E., and Howell S.H. The virulent satellite RNA of Turnip crinkle virus has a major domain homologous to the 3′-end of the helper virus genome. EMBO J. 5 (1986) 3423-3428
71. Simon A.E., Roossinck M.J., and Havelda Z. Plant virus satellite and defective interfering RNAs: new paradigms for a new century. Annu. Rev. Phytopathol. 42 (2004) 415-447
72. Song C., and Simon A.E. Requirement of a 3′-terminal stem-loop in in vitro transcription by an RNA-dependent RNA polymerase. J. Mol. Biol. 254 (1995) 6-14
73. Zhang G., Zhang J., and Simon A.E. Repression and derepression of minus-strand synthesis in a plus-strand RNA virus replicons. J. Virol. 78 (2004) 7619-7633
74. Zhang J., Zhang G., McCormack J.C., and Simon A.E. Evolution of virus-derived sequences for high level replication of a subviral RNA. Virology 351 (2006) 476-488
75. Na H., and White K.A. Structure and prevalence of replication silencer-3′ terminus RNA interactions in Tombusviridae. Virology 345 (2006) 305-316
76. McCormack J.C., Yuan X., Yingling Y.G., Zamora R.E., Shapiro B.A., and Simon A.E. Structural domains within the 3′ UTR of Turnip crinkle virus. J. Virol. 82 (2008) 8706-8720
77. Carpenter C.D., and Simon A.E. Analysis of sequences and putative structures required for viral satellite RNA accumulation by in vivo genetic selection. Nucleic. Acids Res. 26 (1998) 2426-2432
78. Zhang J., Stuntz R.M., and Simon A.E. Analysis of a viral replication repressor: sequence requirements in the large symmetrical loop. Virology 326 (2004) 90-102
79. Zhang J., and Simon A.E. Importance of sequence and structural elements within a viral replication repressor. Virology 333 (2005) 301-315
80. Zhang J., Zhang G., Guo R., Shapiro B.A., and Simon A.E. A pseudoknot in a pre-active form of a viral RNA is part of a structural switch activating minus-strand synthesis. J. Virol. 80 (2006) 9181-9191
81. Guo R., Lin W., Zhang J., Simon A.E., and Kushner D.B. Structural plasticity and rapid evolution in a viral RNA revealed by in vivo genetic selection. J. Virol. 83 (2009) 927-939
82. Zhang G., Zhang J., George A.T., Baumstark T., and Simon A.E. Conformational changes involved in initiation of minus-strand synthesis of a virus-associated RNA. RNA 12 (2006) 147-162
83. Stupina V.A., Meskauskas A., McCormack J.C., Yingling Y.G., Kasprzak W., Shapiro B.A., Dinman J.D., and Simon A.E. The 3′ proximal translational enhancer of Turnip crinkle virus binds to 60S ribosomal subunits. RNA 14 (2008) 2379-2393
84. D'Souza V., and Summers M.F. Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus. Nature 431 (2004) 586-590
85. Rein A. Take two. Nat. Struct. Mol. Biol. 11 (2004) 1034-1035
86. Abbink T.E., Ooms M., Haasnoot P.C., and Berkhout B. The HIV-1 leader RNA conformational switch regulates RNA dimerization but does not regulate mRNA translation. Biochemistry 44 (2005) 9058-9066
87. Paillart J.C., Shehu-Xhilaga M., Marquet R., and Mak J. Dimerization of retroviral RNA genomes: an inseparable pair. Nat. Rev. Microbiol. 2 (2004) 461-472
88. Shen L.X., Cai Z., and Tinoco I. RNA structure at high resolution. FASEB J. 9 (1995) 1023-1033
89. Kao S., Calman A.F., Luciw P.A., and Peterlin B.M. Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature 330 (1987) 489-493
90. Anand K., Schulte A., Vogel-Bachmayr K., Scheffzek K., and Geyer M. Structural insights into the cyclin T1-Tat-TAR RNA transcription activation complex from EIAV. Nat. Struct. Mol. Biol. 15 (2008) 1287-1292
91. Taube R., Fujinaga K., Wimmer J., Barboric M., and Peterlin B.M. Tat transactivation: a model for the regulation of eukaryotic transcriptional elongation. Virology 264 (1999) 245-253
92. Puglisi J.D., Chen L., Blanchard S., and Frankel A.D. Solution structure of a bovine immunodeficiency virus Tat-TAR peptide-RNA complex. Science 270 (1995) 1200-1203
93. Puglisi J.D., Tan R., Calnan B.J., Frankel A.D., and Williamson J.R. Conformation of the TAR RNA-arginine complex by NMR spectroscopy. Science 257 (1992) 76-80
94. Abbink T.E., and 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 (2003) 11601-11611
95. Huthoff H., and Berkhout B. Two alternating structures of the HIV-1 leader RNA. RNA 7 (2001) 143-157
96. Ooms M., Huthoff H., Russell R., Liang C., and Berkhout B. A riboswitch regulates RNA dimerization and packaging in human immunodeficiency virus type 1 virions. J. Virol. 78 (2004) 10814-10819
97. Mihailescu M.R., and Marino J.P. A proton-coupled dynamic conformational switch in the HIV-1 dimerization initiation site kissing complex. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 1189-1194
98. Paillart J.C., Dettenhofer M., Yu X.F., Ehresmann C., Ehresmann B., and Marquet R. First snapshots of the HIV-1 RNA structure in infected cells and in virions. J. Biol. Chem. 279 (2004) 48397-48403
99. Wilkinson K.A., Gorelick R.J., Vasa S.M., Guex N., Rein A., Mathews D.H., Giddings M.C., and Weeks K.M. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol. 6 (2008) 883-899
100. Damgaard C.K., Andersen E.S., Knudsen B., Gorodkin J., and Kjems J. RNA interactions in the 5′ region of the HIV-1 genome. J. Mol. Biol. 336 (2004) 369-379
101. Badorrek C.S., Gherghe C.M., and Weeks K.M. Structure of an RNA switch that enforces stringent retroviral genomic RNA dimerization. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 13640-13645
102. Hahn C.S., Hahn Y.S., Rice C.M., Lee E., Dalgarno L., Strauss E.G., and Strauss J.H. Conserved elements in the 3′ untranslated region of flavivirus RNAs and potential cyclization sequences. J. Mol. Biol. 198 (1987) 33-41
103. Khromykh A.A., Meka H., Guyatt K.J., and Westaway E.G. Essential role of cyclization sequences in flavivirus RNA replication. J. Virol. 75 (2001) 6719-6728
104. Alvarez D.E., Lodeiro M.F., Luduena S.J., Pietrasanta L.I., and Gamarnik A.V. Long-range RNA-RNA interactions circularize the dengue virus genome. J. Virol. 79 (2005) 6631-6643
105. You S., Falgout B., Markoff L., and Padmanabhan R. In vitro RNA synthesis from exogenous dengue viral RNA templates requires long range interactions between 5′- and 3′-terminal regions that influence RNA structure. J. Biol. Chem. 276 (2001) 15581-15591
106. You S., and Padmanabhan R. A novel in vitro replication system for Dengue virus. Initiation of RNA synthesis at the 3′-end of exogenous viral RNA templates requires 5′- and 3′-terminal complementary sequence motifs of the viral RNA. J. Biol. Chem. 274 (1999) 33714-33722
107. Edgil D., and Harris E. End-to-end communication in the modulation of translation by mammalian RNA viruses. Virus Res. 119 (2006) 43-51
108. Filomatori C.V., Lodeiro M.F., Alvarez D.E., Samsa M.M., Pietrasanta L., and Gamarnik A.V. A 5′ RNA element promotes dengue virus RNA synthesis on a circular genome. Genes Dev. 20 (2006) 2238-2249
109. Holden K.L., Stein D.A., Pierson T.C., Ahmed A.A., Clyde K., Iversen P.L., and Harris E. Inhibition of dengue virus translation and RNA synthesis by a morpholino oligomer targeted to the top of the terminal 3′ stem-loop structure. Virology 344 (2006) 439-452
110. Gamarnik A.V., and Andino R. Switch from translation to RNA replication in a positive-stranded RNA virus. Genes Dev. 12 (1998) 2293-2304
111. Alvarez D.E., Filomatori C.V., and Gamarnik A.V. Functional analysis of dengue virus cyclization sequences located at the 5′ and 3′ UTRs. Virology 375 (2008) 223-235
112. Wu B., Pogany J., Na H., Nicholson B.L., Nagy P.D., and White K.A. A discontinuous RNA platform mediates RNA virus replication: building an integrated model for RNA-based regulation of viral processes. PLoS Path. 5 (2009) e1000323
113. Chiu W.W., Kinney R.M., and Dreher T.W. Control of translation by the 5′- and 3′-terminal regions of the dengue virus genome. J. Virol. 79 (2005) 8303-8315
114. Edgil D., Polacek C., and Harris E. Dengue virus utilizes a novel strategy for translation initiation when cap-dependent translation is inhibited. J. Virol. 80 (2006) 2976-2986
115. Bol J.F., Van Vloten-Doting L., and Jaspars E.M.J. A functional equivalence of top component a RNA and coat protein in the initiation of infection by Alfalfa mosaic virus. Virology 46 (1971) 73-85
116. Houwing C.J., and Jaspars E.M.J. Coat protein binds to the 3′-terminal part of RNA 4 of Alfalfa mosaic virus. Biochemistry 17 (1978) 2927-2933
117. Sacher R., and Ahlquist P. Effects of deletions in the N-terminal basic arm of brome mosaic virus coat protein on RNA packaging and systemic infection. J. Virol. 63 (1989) 4545-4552
118. Fukuyama K., Abdel-Meguid S.S., and Rossmann M.G. Crystallization of Alfalfa mosaic virus coat protein as a T = 1 aggregate. J. Mol. Biol. 150 (1981) 33-41
119. Bol J.F., Kraal B., and Brederode F.T. Limited proteolysis of Alfalfa mosaic virus: influence on the structural and biological function of the coat protein. Virology 58 (1974) 101-110
120. Gomila R.C., and Gehrke L. Biochemical approaches for characterizing RNA-protein complexes in preparation for high resolution structure analysis. Methods Mol. Biol. 451 (2008) 279-291
121. Houser-Scott F., Ansel-McKinney P.A., Cai J.M., and Gehrke L. In vitro genetic selection analysis of Alfalfa mosaic virus coat protein binding to 3′-terminal AUGC repeats. J. Virol. 71 (1997) 2310-2319
122. Houser-Scott F., Baer M.L., Liem K.F., Cai J.M., and Gehrke L. Nucleotide sequence and structural determinants of specific binding of coat protein or coat protein peptides to the 3′ untranslated region of Alfalfa mosaic virus RNA 4. J. Virol. 68 (1994) 2194-2205
123. Neeleman L., van der Vossen E.A.G., and Bol J.F. Infection of tobacco with Alfalfa mosaic virus cDNAs sheds new light on the early function of the coat protein. Virology 196 (1993) 883-887
124. Baer M., Houser F., Loesch-Fries L.S., and Gehrke L. Specific RNA binding by amino-terminal peptides of Alfalfa mosaic virus coat protein. EMBO J. 13 (1994) 727-735
125. Reusken C.B.E.M., Neeleman L., and Bol J.F. The 3′-untranslated region of Alfalfa mosaic virus RNA 3 contains at least two independent binding sites for viral coat protein. Nucleic. Acids Res. 22 (1994) 1346-1353
126. Ansel-McKinney P., and Gehrke L. RNA determinants of a specific RNA-coat protein peptide interaction in Alfalfa mosaic virus: conservation of homologous features in ilarvirus RNAs. J. Mol. Biol. 278 (1998) 767-785
127. Guogas L.M., Filman D.J., Hogle J.M., and Gehrke L. Cofolding organizes Alfalfa mosaic virus RNA and coat protein for replication. Science 306 (2004) 2108-2111
128. Ansel-McKinney P., Scott S.W., Swanson M., Ge X., and Gehrke L. A plant viral coat protein RNA-binding consensus sequence contains a crucial arginine. EMBO J. 15 (1996) 5077-5084
129. Boyce M., Scott F., Guogas L.M., and Gehrke L. Base-pairing potential identified by in vitro selection predicts the kinked RNA backbone observed in the crystal structure of the Alfalfa mosaic virus RNA-coat protein complex. J. Mol. Recognit. 19 (2006) 68-78
130. Reichert V.L., Choi M., Petrillo J.E., and Gehrke L. Alfalfa mosaic virus coat protein bridges RNA and RNA-dependent RNA polymerase in vitro. Virology 364 (2007) 214-226
131. Petrillo J.E., Rocheleau G., Kelley-Clarke B., and Gehrke L. Evaluation of the conformational switch model for coat protein function in Alfalfa mosaic virus replication. J. Virol. 79 (2005) 5743-5751
132. Krab I.M., Caldwell C., Gallie D.R., and Bol J.F. Coat protein enhances translational efficiency of Alfalfa mosaic virus RNAs and interacts with the eIF4G component of initiation factor eIF4F. J. Gen. Virol. 86 (2005) 1841-1849
133. Olsthoorn R.C., Mertens S., Brederode F.T., and Bol J.F. A conformational switch at the 3′ end of a plant virus RNA regulates viral replication. EMBO J. 18 (1999) 4856-4864
134. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., and Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5 (2004) 730-737
135. Andrejeva J., Childs K.S., Young D.F., Carlos T.S., Stock N., Goodbourn S., and Randall R.E. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 17264-17269
136. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., Foy E., Loo Y.M., Gale M., Akira S., Yonehara S., Kato A., and Fujita T. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175 (2005) 2851-2858
137. Takahasi K., Yoneyama M., Nishihori T., Hirai R., Kumeta H., Narita R., Gale M., Inagaki F., and Fujita T. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol. Cell 29 (2008) 428-440
138. Cui S., Eisenacher K., Kirchhofer A., Brzozka K., Lammens A., Lammens K., Fujita T., Conzelmann K.K., Krug A., and Hopfner K.P. The C-terminal regulatory domain is the RNA 5′-triphosphate sensor of RIG-I. Mol. Cell 29 (2008) 169-179
139. Hornung V., Ellegast J., Kim S., Brzozka K., Jung A., Kato H., Poeck H., Akira S., Conzelmann K.K., Schlee M., Endres S., and Hartmann G. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314 (2006) 994-997
140. Uzri D., and Gehrke L. Nucleotide sequences and modifications that determine RIG-I/RNA binding and signaling activities. J. Virol. 83 (2009) 4174-4184
141. Saito T., Owen D.M., Jiang F., Marcotrigiano J., and Gale M. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454 (2008) 523-527
142. Bamming D., and Horvath C.M. Regulation of signal transduction by enzymatically inactive antiviral RNA helicase proteins MDA5, RIG-I and LGP2. J. Biol. Chem. 284 (2009) 9700-9712
143. Chang T.H., Liao C.L., and Lin Y.L. Flavivirus induces interferon-beta gene expression through a pathway involving RIG-I-dependent IRF-3 and PI3K-dependent NF-kappaB activation. Microbes Infect. 8 (2006) 157-171
144. Li X., Ranjith-Kumar C.T., Brooks M.T., Dharmaiah S., Herr A.B., Kao C., and Li P. The RIG-I like receptor LGP2 recognizes the termini of double-stranded RNA. J. Biol. Chem. (2009) (epub 2009/03/13)
145. Sioud M. Innate sensing of self and non-self RNAs by Toll-like receptors. Trends Mol. Med. 12 (2006) 167-176
146. Sioud M. Single-stranded small interfering RNA are more immunostimulatory than their double-stranded counterparts: a central role for 2′-hydroxyl uridines in immune responses. Eur. J. Immunol. 36 (2006) 1222-1230
147. Pichlmair A., Schulz O., Tan C.P., Naslund T.I., Liljestrom P., Weber F., and Reise Sousa C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314 (2006) 997-1001
148. Loo Y.M., Owen D.M., Li K., Erickson A.K., Johnson C.L., Fish P.M., Carney D.S., Wang T., Ishida H., Yoneyama M., Fujita T., Saito T., Lee W.M., Hagedorn C.H., Lau D.T., Weinman S.A., Lemon S.M., and Gale M. Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 6001-6006