Abstract:
The mechanisms of RNA replication of plus-strand RNA viruses are still unclear. Here, we identified the first promoter element for RNA synthesis described in a flavivirus. Using dengue virus as a model, we found that the viral RdRp discriminates the viral RNA by specific recognition of a 5′ element named SLA. We demonstrated that RNA-RNA interactions between 5′ and 3′ end sequences of the viral genome enhance dengue virus RNA synthesis only in the presence of an intact SLA. We propose a novel mechanism for minus-strand RNA synthesis in which the viral polymerase binds SLA at the 5′ end of the genome and reaches the site of initiation at the 3′ end via long-range RNA-RNA interactions. These findings provide an explanation for the strict requirement of dengue virus genome cyclization during viral replication. © 2006 by Cold Spring Harbor Laboratory Press.
Registro:
Documento: |
Artículo
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Título: | A 5′ RNA element promotes dengue virus RNA synthesis on a circular genome |
Autor: | Filomatori, C.V.; Lodeiro, M.F.; Alvarez, D.E.; Samsa, M.M.; Pietrasanta, L.; Gamarnik, A.V. |
Filiación: | Fundación Instituto Leloir, Buenos Aires C1405BWE, Argentina Centro de Microscopías Avanzadas, Facultad de Ciencias Exactas Y Naturales, Universidad de Buenos Aires, Buenos Aires C1428BEHA, Argentina Consejo Nacional de Investigaciones Científicas Y Tecnológicas de Argentina, Buenos Aires C1033AAJ, Argentina
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Palabras clave: | AFM; Flavivirus; RNA cyclization; RNA-dependent RNA polymerase; Viral RNA synthesis; article; controlled study; Dengue virus; genome; nonhuman; priority journal; RNA replication; RNA synthesis; RNA virus; atomic force microscopy; biosynthesis; chemistry; conformation; Dengue virus; genetics; metabolism; physiology; regulatory RNA sequence; virus genome; virus replication; Dengue virus; Flavivirus; RNA viruses; NS5 protein, flavivirus; RNA directed RNA polymerase; virus protein; virus RNA; Dengue Virus; Genome, Viral; Microscopy, Atomic Force; Nucleic Acid Conformation; Regulatory Sequences, Ribonucleic Acid; RNA Replicase; RNA, Viral; Viral Nonstructural Proteins; Virus Replication |
Año: | 2006
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Volumen: | 20
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Número: | 16
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Página de inicio: | 2238
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Página de fin: | 2249
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DOI: |
http://dx.doi.org/10.1101/gad.1444206 |
Título revista: | Genes and Development
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Título revista abreviado: | Genes Dev.
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ISSN: | 08909369
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CODEN: | GEDEE
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CAS: | RNA directed RNA polymerase, 9026-28-2; NS5 protein, flavivirus; RNA Replicase, 2.7.7.48; RNA, Viral; Regulatory Sequences, Ribonucleic Acid; Viral Nonstructural Proteins
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PDF: | https://bibliotecadigital.exactas.uba.ar/download/paper/paper_08909369_v20_n16_p2238_Filomatori.pdf |
Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_08909369_v20_n16_p2238_Filomatori |
Referencias:
- Ackermann, M., Padmanabhan, R., De novo synthesis of RNA by the dengue virus RNA-dependent RNA polymerase exhibits temperature dependence at the initiation but not elongation phase (2001) J. Biol. Chem., 276, pp. 39926-39937
- Alvarez, D.E., De Lella Ezcurra, A.L., Fucito, S., Gamarnik, A.V., Role of RNA structures present at the 3′UTR of dengue virus on translation, RNA synthesis, and viral replication (2005) Virology, 339, pp. 200-212
- Alvarez, D.E., Lodeiro, M.F., Ludueña, S.J., Pietrasanta, L.I., Gamarnik, A.V., Long-range RNA-RNA interactions circularize the dengue virus genome (2005) J. Virol., 79, pp. 6631-6643
- Andino, R., Rieckhof, G.E., Baltimore, D., A functional ribonucleoprotein complex forms around the 5′ end of poliovirus RNA (1990) Cell, 63, pp. 369-380
- Brinton, M.A., Fernandez, A.V., Dispoto, J.H., The 3′-nucleotides of flavivirus genomic RNA form a conserved secondary structure (1986) Virology, 153, pp. 113-121
- Cahour, A., Pletnev, A., Vazielle-Falcoz, M., Rosen, L., Lai, C.J., Growth-restricted dengue virus mutants containing deletions in the 5′ noncoding region of the RNA genome (1995) Virology, 207, pp. 68-76
- Corver, J., Lenches, E., Smith, K., Robison, R.A., Sando, T., Strauss, E.G., Strauss, J.H., Fine mapping of a cis-acting sequence element in yellow fever virus RNA that is required for RNA replication and cyclization (2003) J. Virol., 77, pp. 2265-2270
- Dreher, T.W., Functions of the 3′-untranslated regions of positive strand RNA viral genomes (1999) Annu. Rev. Phytopathol., 37, pp. 151-174
- Egloff, M.P., Benarroch, D., Selisko, B., Romette, J.L., Canard, B., An RNA cap (nucleoside-2′-O-)-methyltransferase in the flavivirus RNA polymerase NS5: Crystal structure and functional characterization (2002) EMBO J., 21, pp. 2757-2768
- Elghonemy, S., Davis, W.G., Brinton, M.A., The majority of the nucleotides in the top loop of the genomic 3′ terminal stem loop structure are cis-acting in a West Nile virus infectious clone (2005) Virology, 331, pp. 238-246
- Frolov, I., Hardy, R., Rice, C.M., Cis-acting RNA elements at the 5′ end of Sindbis virus genome RNA regulate minus- and plus-strand RNA synthesis (2001) RNA, 7, pp. 1638-1651
- Gamarnik, A.V., Andino, R., Switch from translation to RNA replication in a positive-stranded RNA virus (1998) Genes & Dev., 12, pp. 2293-2304
- Grdzelishvili, V.Z., Garcia-Ruiz, H., Watanabe, T., Ahlquist, P., Mutual interference between genomic RNA replication and subgenomic mRNA transcription in brome mosaic virus (2005) J. Virol., 79, pp. 1438-1451
- Gubler, D.J., Dengue and dengue hemorrhagic fever (1998) Clin. Microbiol. Rev., 11, pp. 480-496
- Hahn, C.S., Hahn, Y.S., Rice, C.M., Lee, E., Dalgarno, L., Strauss, E.G., Strauss, J.H., Conserved elements in the 3′ untranslated region of flavivirus RNAs and potential cyclization sequences (1987) J. Mol. Biol., 198, pp. 33-41
- Herold, J., Andino, R., Poliovirus RNA replication requires genome circularization through a protein-protein bridge (2001) Mol. Cell, 7, pp. 581-591
- Khromykh, A.A., Meka, H., Guyatt, K.J., Westaway, E.G., Essential role of cyclization sequences in flavivirus RNA replication (2001) J. Virol., 75, pp. 6719-6728
- Kinney, R.M., Butrapet, S., Chang, G.J., Tsuchiya, K.R., Roehrig, J.T., Bhamarapravati, N., Gubler, D.J., Construction of infectious cDNA clones for dengue 2 virus: Strain 16681 and its attenuated vaccine derivative, strain PDK-53 (1997) Virology, 230, pp. 300-308
- Kofler, R.M., Hoenninger, V.M., Thurner, C., Mandl, C.W., Functional analysis of the tick-borne encephalitis virus cyclization elements indicates major differences between mosquito-borne and tick-borne flaviviruses (2006) J. Virol., 80, pp. 4099-4113
- Lo, M.K., Tilgner, M., Bernard, K.A., Shi, P.Y., Functional analysis of mosquito-borne flavivirus conserved sequence elements within 3′ untranslated region of West Nile virus by use of a reporting replicon that differentiates between viral translation and RNA replication (2003) J. Virol., 77, pp. 10004-10014
- McKnight, K.L., Lemon, S.M., The rhinovirus type 14 genome contains an internally located RNA structure that is required for viral replication (1998) RNA, 4, pp. 1569-1584
- Men, R., Bray, M., Clark, D., Chanock, R.M., Lai, C.J., Dengue type 4 virus mutants containing deletions in the 3′ noncoding region of the RNA genome: Analysis of growth restriction in cell culture and altered viremia pattern and immunogenicity in rhesus monkeys (1996) J. Virol., 70, pp. 3930-3937
- Niesters, H.G., Strauss, J.H., Defined mutations in the 5′ nontranslated sequence of Sindbis virus RNA (1990) J. Virol., 64, pp. 4162-4168
- Nomaguchi, M., Teramoto, T., Yu, L., Markoff, L., Padmanabhan, R., Requirements for West Nile virus (-)- And (+)-strand subgenomic RNA synthesis in vitro by the viral RNA-dependent RNA polymerase expressed in Escherichia coli (2004) J. Biol. Chem., 279, pp. 12141-12151
- Olsthoorn, R.C., Bol, J.F., Role of an essential triloop hairpin and flanking structures in the 3′ untranslated region of Alfalfa mosaic virus RNA in in vitro transcription (2002) J. Virol., 76, pp. 8747-8756
- Paul, A.V., Rieder, E., Kim, D.W., Van Boom, J.H., Wimmer, E., Identification of an RNA hairpin in poliovirus RNA that serves as the primary template in the in vitro uridylylation of VPg (2000) J. Virol., 74, pp. 10359-10370
- Pogany, J., Fabian, M.R., White, K.A., Nagy, P.D., A replication silencer element in a plus-strand RNA virus (2003) EMBO J., 22, pp. 5602-5611
- Proutski, V., Gould, E.A., Holmes, E.C., Secondary structure of the 3′ untranslated region of flaviviruses: Similarities and differences (1997) Nucleic Acids Res., 25, pp. 1194-1202
- Ranjith-Kumar, C.T., Zhang, X., Kao, C.C., Enhancer-like activity of a brome mosaic virus RNA promoter (2003) J. Virol., 77, pp. 1830-1839
- Rauscher, S., Flamm, C., Mandl, C.W., Heinz, F.X., Stadler, P.F., Secondary structure of the 3′-noncoding region of flavivirus genomes: Comparative analysis of base pairing probabilities (1997) RNA, 3, pp. 779-791
- Ray, D., White, K.A., An internally located RNA hairpin enhances replication of Tomato bushy stunt virus RNAs (2003) J. Virol., 77, pp. 245-257
- Rice, C., Flaviviridae: The viruses and their replication (2001) Fields Virology, 1, pp. 991-1041. , eds. D. Knipe and P. Howley, Lippincott-Raven, Philadelphia
- Rieder, E., Paul, A.V., Kim, D.W., Van Boom, J.H., Wimmer, E., Genetic and biochemical studies of poliovirus cis-acting replication element cre in relation to VPg uridylylation (2000) J. Virol., 74, pp. 10371-10380
- Selisko, B., Dutartre, H., Guillemot, J.C., Debarnot, C., Benarroch, D., Khromykh, A., Despres, P., Canard, B., Comparative mechanistic studies of de novo RNA synthesis by flavivirus RNA-dependent RNA polymerases (2006) Virology, , in press
- Song, C., Simon, A.E., Requirement of a 3′-terminal stem-loop in in vitro transcription by an RNA-dependent RNA polymerase (1995) J. Mol. Biol., 254, pp. 6-14
- Sullivan, M.L., Ahlquist, P., A brome mosaic virus intergenic RNA3 replication signal functions with viral replication protein 1a to dramatically stabilize RNA in vivo (1999) J. Virol., 73, pp. 2622-2632
- Tilgner, M., Deas, T.S., Shi, P.Y., The flavivirus-conserved penta-nucleotide in the 3′ stem-loop of the West Nile virus genome requires a specific sequence and structure for RNA synthesis, but not for viral translation (2005) Virology, 331, pp. 375-386
- Westaway, E.G., Mackenzie, J.M., Khromykh, A.A., Kunjin RNA replication and applications of Kunjin replicons (2003) Adv. Virus Res., 59, pp. 99-140
- You, S., 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 (1999) J. Biol. Chem., 274, pp. 33714-33722
- You, S., Falgout, B., Markoff, L., 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 (2001) J. Biol. Chem., 276, pp. 15581-15591
- Yu, L., Markoff, L., The topology of bulges in the long stem of the flavivirus 3′ stem-loop is a major determinant of RNA replication competence (2005) J. Virol., 79, pp. 2309-2324
- Zeng, L., Falgout, B., Markoff, L., Identification of specific nucleotide sequences within the conserved 3′-SL in the dengue type 2 virus genome required for replication (1998) J. Virol., 72, pp. 7510-7522
Citas:
---------- APA ----------
Filomatori, C.V., Lodeiro, M.F., Alvarez, D.E., Samsa, M.M., Pietrasanta, L. & Gamarnik, A.V.
(2006)
. A 5′ RNA element promotes dengue virus RNA synthesis on a circular genome. Genes and Development, 20(16), 2238-2249.
http://dx.doi.org/10.1101/gad.1444206---------- CHICAGO ----------
Filomatori, C.V., Lodeiro, M.F., Alvarez, D.E., Samsa, M.M., Pietrasanta, L., Gamarnik, A.V.
"A 5′ RNA element promotes dengue virus RNA synthesis on a circular genome"
. Genes and Development 20, no. 16
(2006) : 2238-2249.
http://dx.doi.org/10.1101/gad.1444206---------- MLA ----------
Filomatori, C.V., Lodeiro, M.F., Alvarez, D.E., Samsa, M.M., Pietrasanta, L., Gamarnik, A.V.
"A 5′ RNA element promotes dengue virus RNA synthesis on a circular genome"
. Genes and Development, vol. 20, no. 16, 2006, pp. 2238-2249.
http://dx.doi.org/10.1101/gad.1444206---------- VANCOUVER ----------
Filomatori, C.V., Lodeiro, M.F., Alvarez, D.E., Samsa, M.M., Pietrasanta, L., Gamarnik, A.V. A 5′ RNA element promotes dengue virus RNA synthesis on a circular genome. Genes Dev. 2006;20(16):2238-2249.
http://dx.doi.org/10.1101/gad.1444206