[en] In eukaryotes, the major nuclear export pathway for mature mRNAs uses the dimeric receptor TAP/p15, which is recruited to mRNAs via the multisubunit TREX complex, comprising the THO core and different export adaptors. Viruses that replicate in the nucleus adopt different strategies to hijack cellular export factors and achieve cytoplasmic translation of their mRNAs. No export receptors are known in plants, but Arabidopsis TREX resembles the mammalian complex, with a conserved hexameric THO core associated with ALY and UIEF proteins, as well as UAP56 and MOS11. The latter protein is an orthologue of mammalian CIP29. The nuclear export mechanism for viral mRNAs has not been described in plants. To understand this process, we investigated the export of mRNAs of the pararetrovirus CaMV in Arabidopsis and demonstrated that it is inhibited in plants deficient in ALY, MOS11 and/or TEX1. Deficiency for these factors renders plants partially resistant to CaMV infection. Two CaMV proteins, the coat protein P4 and reverse transcriptase P5, are important for nuclear export. P4 and P5 interact and co-localise in the nucleus with the cellular export factor MOS11. The highly structured 5' leader region of 35S RNAs was identified as an export enhancing element that interacts with ALY1, ALY3 and MOS11 in vitro.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Kubina, Julie ✱; Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, Strasbourg, France
Geldreich, Angèle ✱; Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, Strasbourg, France
GALES, Jón Pol ✱; Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, Strasbourg, France
Baumberger, Nicolas; Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, Strasbourg, France
Bouton, Clément; Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, Strasbourg, France
Ryabova, Lyubov A ; Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, Strasbourg, France
Grasser, Klaus D; Cell Biology & Plant Biochemistry, Biochemistry Centre, University of Regensburg, D-93053 Regensburg, Germany
Keller, Mario; Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, Strasbourg, France
Dimitrova, Maria ; Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg, Strasbourg, France
✱ These authors have contributed equally to this work.
External co-authors :
yes
Language :
English
Title :
Nuclear export of plant pararetrovirus mRNAs involves the TREX complex, two viral proteins and the highly structured 5' leader region.
Centre National de la Recherche Scientifique Ministère de l’Enseignement supérieur, de la Recherche et de l’Innovation German Research Foundation Institut de Biologie Moléculaire des Plantes
Ramanathan, A., Robb, G.B. and Chan, S.-H. (2016) mRNA capping: biological functions and applications. Nucleic Acids Res., 44, 7511-7526.
Girard, C., Will, C.L., Peng, J., Makarov, E.M., Kastner, B., Lemm, I., Urlaub, H., Hartmuth, K. and Lührmann, R. (2012) Post-transcriptional spliceosomes are retained in nuclear speckles until splicing completion. Nat. Commun., 3, 994.
Stewart, M. (2019) Polyadenylation and nuclear export of mRNAs. J. Biol. Chem., 294, 2977-2987.
Delaleau, M. and Borden, K.L.B. (2015) Multiple export mechanisms for mRNAs. Cells, 4, 452-473.
Heath, C.G., Viphakone, N. and Wilson, S.A. (2016) The role of TREX in gene expression and disease. Biochem. J., 473, 2911-2935.
Williams, T., Ngo, L.H. and Wickramasinghe, V.O. (2018) Nuclear export of RNA: different sizes, shapes and functions. Semin. Cell Dev. Biol., 75, 70-77.
Kang, Y., Bogerd, H.P., Yang, J. and Cullen, B.R. (1999) Analysis of the RNA binding specifcity of the human tap protein, a constitutive transport element-specifc nuclear RNA export factor. Virology, 262, 200-209.
Teplova, M., Wohlbold, L., Khin, N.W., Izaurralde, E. and Patel, D.J. (2011) Structure-function studies of nucleocytoplasmic transport of retroviral genomic RNA by mRNA export factor TAP. Nat. Struct. Mol. Biol., 18, 990-998.
Björk, P. and Wieslander, L. (2017) Integration of mRNP formation and export. Cell. Mol. Life Sci., 74, 2875-2897.
Masuda, S., Das, R., Cheng, H., Hurt, E., Dorman, N. and Reed, R. (2005) Recruitment of the human TREX complex to mRNA during splicing. Genes Dev., 19, 1512-1517.
Hautbergue, G.M., Hung, M.-L., Golovanov, A.P., Lian, L.-Y. and Wilson, S.A. (2008) Mutually exclusive interactions drive handover of mRNA from export adaptors to TAP. Proc. Natl. Acad. Sci. U. S. A., 105, 5154-5159.
Hautbergue, G.M., Hung, M.-L., Walsh, M.J., Snijders, A.P.L., Chang, C.-T., Jones, R., Ponting, C.P., Dickman, M.J. and Wilson, S.A. (2009) UIF, a New mRNA export adaptor that works together with REF/A LY, requires FACT for recruitment to mRNA. Curr. Biol., 19, 1918-1924.
Shen, J., Zhang, L. and Zhao, R. (2007) Biochemical characterization of the ATPase and helicase activity of UAP56, an essential pre-mRNA splicing and mRNA export factor. J. Biol. Chem., 282, 22544-22550.
Fukuda, S., Wu, D.W., Stark, K. and Pelus, L.M. (2002) Cloning and characterization of a proliferation-associated cytokine-inducible protein, CIP29. Biochem. Biophys. Res. Commun., 292, 593-600.
Cheng, H., Dufu, K., Lee, C.-S., Hsu, J.L., Dias, A. and Reed, R. (2006) Human mRNA export machinery recruited to the 5' end of mRNA. Cell, 127, 1389-1400.
Chi, B., Wang, Q., Wu, G., Tan, M., Wang, L., Shi, M., Chang, X. and Cheng, H. (2013) Aly and THO are required for assembly of the human TREX complex and association of TREX components with the spliced mRNA. Nucleic Acids Res., 41, 1294-1306.
Viphakone, N., Sudbery, I., Griffth, L., Heath, C.G., Sims, D. and Wilson, S.A. (2019) Co-transcriptional loading of RNA export factors shapes the human transcriptome. Mol. Cell, 75, 310-323.
Le Hir, H., Gatfeld, D., Izaurralde, E. and Moore, M.J. (2001) The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J., 20, 4987-4997.
Dufu, K., Livingstone, M.J., Seebacher, J., Gygi, S.P., Wilson, S.A. and Reed, R. (2010) ATP is required for interactions between UAP56 and two conserved mRNA export proteins, Aly and CIP29, to assemble the TREX complex. Genes Dev., 24, 2043-2053.
Viphakone, N, Hautbergue, GM., Walsh, M., Chang, C.-T, Holland, A., Folco, E.G, Reed, R. and Wilson, S.A. (2012) TREX exposes the RNA-binding domain of Nxf1 to enable mRNA export. Nat. Commun., 3, 1006.
Wickramasinghe, V.O. and Laskey, R.A. (2015) Control of mammalian gene expression by selective mRNA export. Nat. Rev. Mol. Cell Biol, 16, 431-442.
Kiesler, E., Miralles, F. and Visa, N (2002) HEL/UAP56 binds cotranscriptionally to the Balbiani ring pre-mRNA in an intron-independent manner and accompanies the BR mRNP to the nuclear pore. Curr. Biol, 12, 859-862.
Nojima, T, Hirose, T, Kimura, H. and Hagiwara, M. (2007) The interaction between Cap-binding complex and RNA export factor is required for intronless mRNA export. J. Biol. Chem., 282, 15645-15651.
Huang, Y. and Steitz, J.A. (2001) Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol. Cell, 7, 899-905.
Hargous, Y, Hautbergue, GM., Tintaru, A.M., Skrisovska, L., Golovanov, A.P, Stevenin, J., Lian, L.-Y, Wilson, S.A. and Allain, F.H.-T (2006) Molecular basis of RNA recognition and TAP binding by the SR proteins SRp20 and 9G8. EMBO J., 25, 5126-5137.
Tintaru, A.M., Hautbergue, GM., Hounslow, A.M., Hung, M.-L., Lian, L.-Y, Craven, C.J. and Wilson, S.A. (2007) Structural and functional analysis of RNA and TAP binding to SF2/ASF. EMBO Rep., 8, 756-762.
Lei, H., Dias, A.P and Reed, R. (2011) Export and stability of naturally intronless mRNAs require specifc coding region sequences and the TREX mRNA export complex. Proc. Natl. Acad. Sci. U.S.A., 108, 17985-17990.
Lei, H., Zhai, B., Yin, S., Gygi, S. and Reed, R. (2013) Evidence that a consensus element found in naturally intronless mRNAs promotes mRNA export. Nucleic Acids Res., 41, 2517-2525.
Ehrnsberger, H.F., Grasser, M. and Grasser, K.D. (2019) Nucleocytosolic mRNA transport in plants: export factors and their infuence on growth and development. J. Exp. Bot., 70, 3757-3763.
Yelina, NE., Smith, L.M., Jones, A.M.E., Patel, K., Kelly, K.A. and Baulcombe, D.C (2010) Putative Arabidopsis THO/TREX mRNA export complex is involved in transgene and endogenous siRNA biosynthesis. Proc. Natl. Acad. Sci. U.S.A., 107, 13948-13953.
Uhrig, J.F., Canto, T, Marshall, D. and MacFarlane, S.A. (2004) Relocalization of nuclear ALY proteins to the cytoplasm by the tomato bushy stunt virus P19 pathogenicity protein. Plant Physiol, 135, 2411-2423.
Pfaff, C, Ehrnsberger, H.F., Flores-Tornero, M., Sørensen, B.B., Schubert, T, Langst, G, Griesenbeck, J., Sprunck, S., Grasser, M. and Grasser, K.D. (2018) ALY RNA-Binding proteins are required for Nucleocytosolic mRNA transport and modulate plant growth and development1[OPEN]. Plant Physiol, 177, 226-240.
Ehrnsberger, H.F., Pfaff, C, Hachani, I., Flores-Tornero, M., Sørensen, B.B., Langst, G, Sprunck, S., Grasser, M. and Grasser, K.D. (2019) The UAP56-Interacting export factors UIEF1 and UIEF2 function in mRNA export. Plant Physiol, 179, 1525-1536.
Kammel, C, Thomaier, M., Sørensen, B.B., Schubert, T, Langst, G, Grasser, M. and Grasser, K.D. (2013) Arabidopsis DEAD-box RNA helicase UAP56 interacts with both RNA and DNA as well as with mRNA export factors. PLoS One, 8, e60644.
Germain, H., Qu, N., Cheng, Y.T., Lee, E., Huang, Y., Dong, O.X., Gannon, P., Huang, S., Ding, P., Li, Y. et al. (2010) MOS11: a new component in the mRNA export pathway. PLoS Genet., 6, e1001250.
Gales, J.P., Kubina, J., Geldreich, A. and Dimitrova, M. (2020) Strength in diversity: nuclear export of viral RNAs. Viruses, 12, 1014.
Koffa, M.D., Clements, J.B., Izaurralde, E., Wadd, S., Wilson, S.A., Mattaj, I.W. and Kuersten, S. (2001) Herpes simplex virus ICP27 protein provides viral mRNAs with access to the cellular mRNA export pathway. EMBO J., 20, 5769-5778.
Malik, P., Blackbourn, D.J. and Clements, J.B. (2004) The evolutionarily conserved Kaposi's sarcoma-associated herpesvirus ORF57 protein interacts with REF protein and acts as an RNA export factor. J. Biol. Chem., 279, 33001-33011.
Boyne, J.R., Colgan, K.J. and Whitehouse, A. (2008) Herpesvirus saimiri ORF57: a post-transcriptional regulatory protein. Front. Biosci. J. Virtual Libr., 13, 2928-2938.
Tunnicliffe, R.B., Hautbergue, G.M., Kalra, P., Jackson, B.R., Whitehouse, A., Wilson, S.A. and Golovanov, A.P. (2011) Structural basis for the recognition of cellular mRNA export factor REF by herpes viral proteins HSV-1 ICP27 and HVS ORF57. PLoS Pathog., 7, e1001244.
Tunnicliffe, R.B., Tian, X., Storer, J., Sandri-Goldin, R.M. and Golovanov, A.P. (2018) Overlapping motifs on the herpes viral proteins ICP27 and ORF57 mediate interactions with the mRNA export adaptors ALYREF and UIF. Sci. Rep., 8, 15005.
Jackson, B.R., Boyne, J.R., Noerenberg, M., Taylor, A., Hautbergue, G.M., Walsh, M.J., Wheat, R., Blackbourn, D.J., Wilson, S.A. and Whitehouse, A. (2011) An interaction between KSHV ORF57 and UIF provides mRNA-adaptor redundancy in herpesvirus intronless mRNA export. PLoS Pathog., 7, e1002138.
Schumann, S., Baquero-Perez, B. and Whitehouse, A. (2016) Interactions between KSHV ORF57 and the novel human TREX proteins, CHTOP and CIP29. J. Gen. Virol., 97, 1904-1910.
Grüter, P., Tabernero, C., von Kobbe, C., Schmitt, C., Saavedra, C., Bachi, A., Wilm, M., Felber, B.K. and Izaurralde, E. (1998) TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell, 1, 649-659.
Chi, B., Wang, K., Du, Y., Gui, B., Chang, X., Wang, L., Fan, J., Chen, S., Wu, X., Li, G. et al. (2014) A sub-element in PRE enhances nuclear export of intronless mRNAs by recruiting the TREX complex via ZC3H18. Nucleic Acids Res., 42, 7305-7318.
Karsies, A., Merkle, T., Szurek, B., Bonas, U., Hohn, T. and Leclerc, D. (2002) Regulated nuclear targeting of caulifower mosaic virus. J. Gen. Virol., 83, 1783-1790.
Haas, M., Geldreich, A., Bureau, M., Dupuis, L., Leh, V., Vetter, G., Kobayashi, K., Hohn, T., Ryabova, L., Yot, P. et al. (2005) The open reading frame VI product of Caulifower mosaic virus is a nucleocytoplasmic protein: its N terminus mediates its nuclear export and formation of electron-dense viroplasms. Plant Cell, 17, 927-943.
Kiss-László, Z., Blanc, S. and Hohn, T. (1995) Splicing of caulifower mosaic virus 35S RNA is essential for viral infectivity. EMBO J., 14, 3552-3562.
Bouton, C., Geldreich, A., Ramel, L., Ryabova, L.A., Dimitrova, M. and Keller, M. (2015) Caulifower mosaic virus transcriptome reveals a complex alternative splicing pattern. PLoS One, 10, e0132665.
Torruella, M., Gordon, K. and Hohn, T. (1989) Caulifower mosaic virus produces an aspartic proteinase to cleave its polyproteins. EMBO J., 8, 2819-2825.
Ryabova, L., Park, H.-S. and Hohn, T. (2004) Control of translation reinitiation on the caulifower mosaic virus (CaMV) polycistronic RNA. Biochem. Soc. Trans., 32, 592-596.
Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant., 15, 473-497.
Li, H., Shen, J.J., Zheng, Z.L., Lin, Y. and Yang, Z. (2001) The Rop GTPase switch controls multiple developmental processes in Arabidopsis. Plant Physiol., 126, 670-684.
Sørensen, B.B., Ehrnsberger, H.F., Esposito, S., Pfab, A., Bruckmann, A., Hauptmann, J., Meister, G., Merkl, R., Schubert, T., Längst, G. et al. (2017) The Arabidopsis THO/TREX component TEX1 functionally interacts with MOS11 and modulates mRNA export and alternative splicing events. Plant Mol. Biol., 93, 283-298.
Lellis, A.D., Kasschau, K.D., Whitham, S.A. and Carrington, J.C. (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr. Biol., 12, 1046-1051.
Yoo, S.-D., Cho, Y.-H. and Sheen, J. (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc., 2, 1565-1572.
Dimitrova, M., Imbert, I., Kieny, M.P. and Schuster, C. (2003) Protein-protein interactions between hepatitis C virus nonstructural proteins. J. Virol., 77, 5401-5414.
Kim, G.-D., Cho, Y.-H. and Yoo, S.-D. (2017) Regulatory functions of cellular energy sensor SNF1-Related Kinase1 for leaf senescence delay through ETHYLENE-INSENSITIVE3 Repression. Sci. Rep., 7, 3193.
Link, D., Schmidlin, L., Schirmer, A., Klein, E., Erhardt, M., Geldreich, A., Lemaire, O. and Gilmer, D. (2005) Functional characterization of the Beet necrotic yellow vein virus RNA-5-encoded p26 protein: evidence for structural pathogenicity determinants. J. Gen. Virol., 86, 2115-2125.
Khelifa, M., Massé, D., Blanc, S. and Drucker, M. (2010) Evaluation of the minimal replication time of Caulifower mosaic virus in different hosts. Virology, 396, 238-245.
Sorek, N., Gutman, O., Bar, E., Abu-Abied, M., Feng, X., Running, M.P., Lewinsohn, E., Ori, N., Sadot, E., Henis, Y.I. et al. (2011) Differential effects of prenylation and s-acylation on type I and II ROPS membrane interaction and function. Plant Physiol., 155, 706-720.
Revers, F. and García, J.A. (2015) Molecular biology of potyviruses. Adv. Virus Res., 92, 101-199.
Schepetilnikov, M., Kobayashi, K., Geldreich, A., Caranta, C., Robaglia, C., Keller, M. and Ryabova, L.A. (2011) Viral factor TAV recruits TOR/S6K1 signalling to activate reinitiation after long ORF translation. EMBO J., 30, 1343-1356.
Thiébeauld, O., Schepetilnikov, M., Park, H.-S., Geldreich, A., Kobayashi, K., Keller, M., Hohn, T. and Ryabova, L.A. (2009) A new plant protein interacts with eIF3 and 60S to enhance virus-activated translation re-initiation. EMBO J., 28, 3171-3184.
Angel, C.A., Lutz, L., Yang, X., Rodriguez, A., Adair, A., Zhang, Y., Leisner, S.M., Nelson, R.S. and Schoelz, J.E. (2013) The P6 protein of caulifower mosaic virus interacts with CHUP1, a plant protein which moves chloroplasts on actin microflaments. Virology, 443, 363-374.
Amari, K., Boutant, E., Hofmann, C., Schmitt-Keichinger, C., Fernandez-Calvino, L., Didier, P., Lerich, A., Mutterer, J., Thomas, C.L., Heinlein, M. et al. (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog., 6, e1001119.
Bonneville, J.M., Sanfaçon, H., Fütterer, J. and Hohn, T. (1989) Posttranscriptional trans-activation in caulifower mosaic virus. Cell, 59, 1135-1143.
Gowda, S., Wu, F.C., Scholthof, H.B. and Shepherd, R.J. (1989) Gene VI of fgwort mosaic virus (caulimovirus group) functions in posttranscriptional expression of genes on the full-length RNA transcript. Proc. Natl. Acad. Sci. U.S.A., 86, 9203-9207.
Fütterer, J., Gordon, K., Sanfaçon, H., Bonneville, J.M. and Hohn, T. (1990) Positive and negative control of translation by the leader sequence of caulifower mosaic virus pregenomic 35S RNA. EMBO J., 9, 1697-1707.
Scholthof, H.B., Gowda, S., Wu, F.C. and Shepherd, R.J. (1992) The full-length transcript of a caulimovirus is a polycistronic mRNA whose genes are trans activated by the product of gene VI. J. Virol., 66, 3131-3139.
Takatsuji, H., Yamauchi, H., Watanabe, S., Kato, H. and Ikeda, J.E. (1992) Caulifower mosaic virus reverse transcriptase. Activation by proteolytic processing and functional alteration by terminal deletion. J. Biol. Chem., 267, 11579-11585.
Ani, R.A., Pfeiffer, P., Lebeurier, G. and Hirth, L. (1979) The structure of caulifower mosaic virus I. pH-Induced structural changes. Virology, 93, 175-187.
Martinez-Izquierdo, J. and Hohn, T. (1987) Caulifower mosaic virus coat protein is phosphorylated in vitro by a virion-associated protein kinase. Proc. Natl. Acad. Sci. U.S.A., 84, 1824-1828.
Karsies, A., Hohn, T. and Leclerc, D. (2001) Degradation signals within both terminal domains of the caulifower mosaic virus capsid protein precursor. Plant J., 27, 335-343.
Pfeiffer, P., Laquel, P. and Hohn, T. (1984) Caulifower mosaic virus replication complexes: characterization of the associated enzymes and of the polarity of the DNA synthesized in vitro. Plant Mol. Biol., 3, 261-270.
Haseloff, J. and Siemering, K. (1998) The uses of green fuorescent protein in plants. In: Chalfe, M. and Kain, S. (eds). Green Fluorescent Protein: Properties, Applications and Protocols. Wiley-Liss, Inc., NY, pp. 191-220.
Hanson, M.R. and Köhler, R.H. (2001) GFP imaging: methodology and application to investigate cellular compartmentation in plants. J. Exp. Bot., 52, 529-539.
Champagne, J., Benhamou, N. and Leclerc, D. (2004) Localization of the N-terminal domain of caulifower mosaic virus coat protein precursor. Virology, 324, 257-262.
Kosugi, S., Hasebe, M., Tomita, M. and Yanagawa, H. (2009) Systematic identifcation of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. U.S.A., 106, 10171-10176.
Sperschneider, J., Catanzariti, A.-M., DeBoer, K., Petre, B., Gardiner, D.M., Singh, K.B., Dodds, P.N. and Taylor, J.M. (2017) LOCALIZER: subcellular localization prediction of both plant and effector proteins in the plant cell. Sci. Rep., 7, 44598.
Haas, G., Azevedo, J., Moissiard, G., Geldreich, A., Himber, C., Bureau, M., Fukuhara, T., Keller, M. and Voinnet, O. (2008) Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. EMBO J., 27, 2102-2112.
Pooggin, M.M. and Ryabova, L.A. (2018) Ribosome shunting, polycistronic translation, and evasion of antiviral defenses in plant pararetroviruses and beyond. Front. Microbiol., 9, 644.
Hemmings-Mieszczak, M., Steger, G. and Hohn, T. (1997) Alternative structures of the caulifower mosaic virus 35 S RNA leader: implications for viral expression and replication. J. Mol. Biol., 267, 1075-1088.
Hohn, T. and Rothnie, H. (2013) Plant pararetroviruses: replication and expression. Curr. Opin. Virol., 3, 621-628.
Guerra-Peraza, O., de Tapia, M., Hohn, T. and Hemmings-Mieszczak, M. (2000) Interaction of the caulifower mosaic virus coat protein with the pregenomic RNA leader. J. Virol., 74, 2067-2072.
Pfeiffer, P. and Hohn, T. (1983) Involvement of reverse transcription in the replication of caulifower mosaic virus: a detailed model and test of some aspects. Cell, 33, 781-789.
Williams, B.J.L., Boyne, J.R., Goodwin, D.J., Roaden, L., Hautbergue, G.M., Wilson, S.A. and Whitehouse, A. (2005) The prototype gamma-2 herpesvirus nucleocytoplasmic shuttling protein, ORF 57, transports viral RNA through the cellular mRNA export pathway. Biochem. J., 387, 295-308.
Chaudhary, S., Khokhar, W., Jabre, I., Reddy, A.S.N., Byrne, L.J., Wilson, C.M. and Syed, N.H. (2019) Alternative splicing and protein diversity: plants versus animals. Front. Plant Sci., 10, 708.
Fütterer, J., Gordon, K., Bonneville, J.M., Sanfaçon, H., Pisan, B., Penswick, J. and Hohn, T. (1988) The leading sequence of caulimovirus large RNA can be folded into a large stem-loop structure. Nucleic Acids Res., 16, 8377-8390.
Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
Köhler, A. and Hurt, E. (2007) Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol., 8, 761-773.
Pan, H., Liu, S. and Tang, D. (2012) HPR1, a component of the THO/TREX complex, plays an important role in disease resistance and senescence in Arabidopsis. Plant J. Cell Mol. Biol., 69, 831-843.
Xu, C., Zhou, X. and Wen, C.-K. (2015) HYPER RECOMBINATION1 of the THO/TREX complex plays a role in controlling transcription of the REVERSION-TO-ETHYLENE SENSITIVITY1 gene in Arabidopsis. PLos Genet., 11, e1004956.
Strässer, K. and Hurt, E. (2000) Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J., 19, 410-420.
Zenklusen, D., Vinciguerra, P., Strahm, Y. and Stutz, F. (2001) The yeast hnRNP-Like proteins Yra1p and Yra2p participate in mRNA export through interaction with Mex67p. Mol. Cell. Biol., 21, 4219-4232.
Kang, Y. and Cullen, B.R. (1999) The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev., 13, 1126-1139.
LeBlanc, J.J., Uddowla, S., Abraham, B., Clatterbuck, S. and Beemon, K.L. (2007) Tap and Dbp5, but not Gag, are involved in DR-mediated nuclear export of unspliced Rous sarcoma virus RNA. Virology, 363, 376-386.
Sakuma, T., Davila, J.I., Malcolm, J.A., Kocher, J.-P.A., Tonne, J.M. and Ikeda, Y. (2014) Murine leukemia virus uses NXF1 for nuclear export of spliced and unspliced viral transcripts. J. Virol., 88, 4069-4082.
Pessel-Vivares, L., Houzet, L., Lainé, S. and Mougel, M. (2015) Insights into the nuclear export of murine leukemia virus intron-containing RNA. RNA Biol., 12, 942-949.
Mougel, M., Akkawi, C., Chamontin, C., Feuillard, J., Pessel-Vivares, L., Socol, M. and Laine, S. (2020) NXF1 and CRM1 nuclear export pathways orchestrate nuclear export, translation and packaging of murine leukaemia retrovirus unspliced RNA. RNA Biol., 17, 528-538.
Flint, S.J., Huang, W., Goodhouse, J. and Kyin, S. (2005) A peptide inhibitor of exportin1 blocks shuttling of the adenoviral E1B 55 kDa protein but not export of viral late mRNAs. Virology, 337, 7-17.
Yatherajam, G., Huang, W. and Flint, S.J. (2011) Export of adenoviral late mRNA from the nucleus requires the Nxf1/Tap export receptor. J. Virol., 85, 1429-1438.
Johnson, L.A., Li, L. and Sandri-Goldin, R.M. (2009) The cellular RNA export receptor TAP/NXF1 is required for ICP27-mediated export of herpes simplex virus 1 RNA, but the TREX complex adaptor protein Aly/REF appears to be dispensable. J. Virol., 83, 6335-6346.
Tian, X., Devi-Rao, G., Golovanov, A.P. and Sandri-Goldin, R.M. (2013) The interaction of the cellular export adaptor protein Aly/REF with ICP27 contributes to the effciency of herpes simplex virus 1 mRNA export. J. Virol., 87, 7210-7217.
Heise, T., Sommer, G., Reumann, K., Meyer, I., Will, H. and Schaal, H. (2006) The hepatitis B virus PRE contains a splicing regulatory element. Nucleic Acids Res., 34, 353-363.
Lee, G.H., Wasser, S. and Lim, S.G. (2008) Hepatitis B pregenomic RNA splicing-The products, the regulatory mechanisms and its biological signifcance. Virus Res., 136, 1-7.
Sommer, G. and Heise, T. (2008) Posttranscriptional control of HBV gene expression. Front. Biosci. J. Virtual Libr., 13, 5533-5547.
Hernandez, F.P. and Sandri-Goldin, R.M. (2010) Head-to-tail intramolecular interaction of herpes simplex virus type 1 regulatory protein ICP27 is important for its interaction with cellular mRNA export receptor TAP/NXF1. mBio, 1, e00268-10.
Diot, C., Fournier, G., Dos Santos, M., Magnus, J., Komarova, A., van der Werf, S., Munier, S. and Naffakh, N. (2016) Infuenza A virus polymerase recruits the RNA helicase DDX19 to promote the nuclear export of viral mRNAs. Sci. Rep., 6, 33763.
Ren, X., Yu, Y., Li, H., Huang, J., Zhou, A., Liu, S., Hu, P., Li, B., Qi, W. and Liao, M. (2019) Avian infuenza A virus polymerase recruits cellular RNA helicase eIF4A3 to promote viral mRNA splicing and spliced mRNA nuclear export. Front. Microbiol., 10, 1625.
Marsh, L.E. and Guilfoyle, T.J. (1987) Caulifower mosaic virus replication intermediates are encapsidated into virion-like particles. Virology, 161, 129-137.
Himmelbach, A., Chapdelaine, Y. and Hohn, T. (1996) Interaction between caulifower mosaic virus inclusion body protein and capsid protein: implications for viral assembly. Virology, 217, 147-157.
Menissier, J., Laquel, P., Lebeurier, G. and Hirth, L. (1984) A DNA polymerase activity is associated with Caulifower Mosaic Virus. Nucleic Acids Res., 12, 8769-8778.
Haas, M., Bureau, M., Geldreich, A., Yot, P. and Keller, M. (2002) Caulifower mosaic virus: still in the news. Mol. Plant Pathol., 3, 419-429.
Kobayashi, K., Nakayashiki, H., Tsuge, S., Mise, K. and Furusawa, I. (1998) Accumulation kinetics of viral gene products in caulifower mosaic virus-infected turnip protoplasts. Microbiol. Immunol., 42, 65-69.
Li, H.-C., Huang, E.-Y., Su, P.-Y., Wu, S.-Y., Yang, C.-C., Lin, Y.-S., Chang, W.-C. and Shih, C. (2010) Nuclear export and import of human hepatitis B virus capsid protein and particles. PLoS Pathog., 6, e1001162.
