Abstract
The function of the nxf1 (Nuclear Export Factor 1) gene is the nuclear-cytoplasmic transport of most mRNAs. A characteristic feature of the nxf1 genes in animals belonging to different taxonomic groups is existence of an alternative transcript with a homologous intron referred to as a cassette intron. The following databases were used: GenBank (http://www.ncbi.nlm.nih.gov/); FlyBase (http://flybase.org/); and UCSC Genome (http://genome.ucsc.edu). To build secondary structures of nucleotide sequences we used a UNAFold v3.8 suite (http://mfold.rna.albany.edu/). The nxf1 cassette introns form characteristic secondary structures. The paper discusses the possible functional significance of the intron-retaining transcripts of the nxf1 genes.
Similar content being viewed by others
References
Bachi, A., Braun, I.C., Rodrigues, J.P., et al., The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates, RNA, 2000, vol. 6, pp. 136–158.
Bashirullah, A., Cooperstock, R.L., and Lipshitz, H.D., RNA localization in development, Annu. Rev. Biochem., 1998, vol. 67, pp. 335–394.
Behm-Ansmant, I., Gatfield, D., Rehwinkel, J., et al., A conserved role for cytoplasmic poly (A)-binding protein 1 (PABPC1) in nonsense-mediated mRNA, EMBO J., 2007, vol. 26, pp. 1–11.
Besse, F. and Ephrussi, A., Translational control of localized mRNAs: restricting protein synthesis in space and time, Nature Rev., 2008, vol. 9, pp. 971–980.
Black, D.L. and Grabowski, P.J., Alternative premRNA splicing and neuronal function, Prog. Mol. Subcell. Biol., 2003, vol. 31, pp. 187–216.
Blencowe, B.J., Exonic splicing enhancers: mechanism of action, diversity and role in human disease, Trends Biochem. Sci., 2000, vol. 25, pp. 106–110.
Boutz, P.L., Stoilov, P., Li, Q., et al., A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons, Genes Develop., 2007, vol. 21, pp. 1636–1652.
Braun, I.C., Rohrbach, E., Schmitt, C., and Izaurralde, E., Tap binds to the constitutive transport element (CNE) through a novel RNA binding motif that is sufficient to promote CTE-dependent RNA export from the nucleus, EMBO J., 1999, vol. 18, pp. 1953–1965.
Burge, C.B., Tuschl, T., and Sharp, P.A., Splicing of precursors of mRNAs by the spliceosomes, in The RNA World, Gesteland, R.F., et al., Eds., Cold Spring Harbor, New York: Cold Spring Harbor Lab. Press., 1999, pp. 525–560.
Cavalier-Smith, T., Intron phylogeny: a new hypothesis, Trends Genet., 1991, vol. 7, pp. 145–148.
Coyle, J.H., Guzik, B.W., Bor, Y.-C., et al., Sam68 enhances the cytoplasmic utilization of intron-containing RNA and is functionally regulated by the nuclear kinase Sik/BRK, Mol. Cell Biol., 2003, vol. 23, pp. 92–103.
Darnell, J.E. and Doolittle, W.F., Speculations on the early course of evolution, Proc. Natl. Acad. Sci. USA, 1986, vol. 83, pp. 1271–1275.
David, A., Dolan, B.P., Hickman, H.D., et al., Nuclear translation visualized by ribosome-bound nascent chain puromycylation, J. Cell Biol., 2012, vol. 197, pp. 45–57.
Dehay, C. and Kennedy, H., Transcriptional regulation and alternative splicing make for better brains, Neuron, 2009, vol. 62, pp. 455–457.
Faustino, N.A. and Cooper, T.A., Pre-mRNA splicing and human disease, Genes Dev., 2003, vol. 17, pp. 419–437.
Fedorova, L. and Fedorov, A., Introns in gene evolution, Genetics, 2003, vol. 118, pp. 123–131.
Forrest, S.T., Barringhaus, K.G., and Perlegas, D., Intron retention generates a novel id3 isoform that inhibits vascular lesion formation, J. Biol. Chem., 2004, vol. 279, pp. 32897–32903.
Frints, S.G., Jun, L., Fryns, J.P., et al., Inv (X) (p21.1; q22.1) in a man with mental retardation, short stature, general muscle wasting, and facial dysmorphism: clinical study and mutation analysis of the NXF5 gene, Amer. J. Med. Genet., 2003, vol. 119, pp. 367–374.
Galante, P.A., Sakabe, N.J., Kirschbaum-Slager, N., and de Souza, S.J., Detection and evaluation of intron retention events in the human transcriptome, RNA, 2004, vol. 10, pp. 757–765.
Gatfield, D., Unterholzner, L., Ciccarelli, F.D., et al., Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways, EMBO J., 2003, vol. 22, pp. 3960–3970.
Gatfield, D. and Izaurralde, E., Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila, Nature, 2004, vol. 429, pp. 575–578.
Gilbert, W., Why genes in pieces?, Nature, 1978, vol. 271, p. 501.
Gilbert, W., Origin of life: the RNA world, Nature, 1986, vol. 319, p. 618.
Golubkova, E.V. and Mamon, L.A., The role of Dm NXF1 in controlling early embryonic mitoses in Drosophila melanogaster, in Cell Division: Theory, Variants, and Degradation, Golitsin, Y.N. and Krylov, M.C., Eds., Nova Science Publishers, Inc., 2010, pp. 127–132.
Golubkova, E., Mamon, L., Nikulina, A., et al., The evolutionarily conserved family of nuclear export factor (NXF) in Drosophila melanogaster, in Drosophila melanogaster: Life Cycle, Genetics and Development, Spindler-Barth, M., Ed., Nova Science Publishers, Inc., 2012, pp. 63–82.
Gonzalez, C.I., Ruiz-Echevarria, M.J., Vasudevan, S., et al., The yeast hnRNP-like protein Hrp1/Nab4 marks a transcript for nonsense-mediated mRNA decay, Mol. Cell, 2000, vol. 5, pp. 489–499.
Graveley, B.R., Alternative splicing: increasing diversity in the proteomic world, Trends Genet., 2001, vol. 17, pp. 100–107.
Grillo, L., Reitano, S., Belfiore, G., et al., Familial 1.1 mb deletion in chromosome xq22.1 associated with mental retardation and behavioural disorders in female patients, Europ. J. Med. Genet, 2010, vol. 53, pp. 113–116.
Grosso, A.R., Gomes, A.Q., Barbosa-Morais, N.L., et al., Tissue-specific splicing factor gene expression signatures, Nucleic Acids Res., 2008, vol. 36, pp. 4823–4832.
Grüter, P., Tabemero, C., von Kobbe, C., et al., Tap, human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus, Mol. Cell, 1998, vol. 1, pp. 649–659.
Guzik, B.W., Levesque, L., Prasad, S., et al., NTF1 (p15) is a crucial cellular cofactor in tap-dependent export of intron-containing RNA in mammalian cells, Mol. Cell. Biol., 2001, vol. 21, pp. 2545–2554.
Hansen, K.D., Lareau, L.F., Blanchette, M., et al., Genome-wide identification of alternative splice forms down-regulated by nonsense-mediated mRNA decay in Drosophila, PLoS Genetics, 2009, vol. 5, p. e1000525.
Herold, A., Suyama, M., Rodrigues, J.P., et al., TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture, Mol. Cell Biol., 2000, vol. 20, pp. 8996–9008.
Herold, A., Klymenko, T., and Izaurralde, E., NXF1/p15 heterodimers are essential for mRNA nuclear export in Drosophila, RNA, 2001, vol. 7, pp. 1768–1780.
Herold, A., Teixeira, L., and Izaurralde, E., Genome-wide analysis of nuclear mRNA export pathways in Drosophila, EMBO J., 2003, vol. 22, pp. 2472–2483.
Huang, Y.-S., Carson, J.H., Barbarese, E., and Richter, J.D., Facilitation of dendritic mRNA transport by CPEB, Gene Dev., 2003, vol. 17, pp. 638–653.
Ivankova, N., Tretyakova, I., Lyozin, G., et al., Alternative transcripts expressed by small bristles, the Drosophila melanogaster nxf 1 gene, Gene, 2010, vol. 458, pp. 11–19.
Jun, L., Frints, S., Duhamel, H., et al., Nxf5, a novel member of the nuclear RNA export factor family, is lost in a male patient with a syndromic form of mental retardation, Curr. Biol, 2001, vol. 11, pp. 1381–1391.
Kan, Z., States, D., and Gish, W., Selecting for functional alternative splices in ESTs, Genome Res., 2002, vol. 12, pp. 1837–1845.
Kosik, K.S. and Krichevsky, A.M., The message and the messenger: delivering RNA in neurons, Sci. STKE, 2002, vol. 126, pp. 1–4.
Kozak, M., Regulation of translation via mRNA structure in prokaryotes and eukaryotes, Gene, 2005, vol. 361, pp. 13–37.
Krichevsky, A.M. and Kosik, K.S., Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation, Neuron, 2001, vol. 32, pp. 683–696.
Lareau, L.F., Green, R.E., Bhatnagar, R.S., and Brenner, S.E., The evolving roles of alternative splicing, Curr. Opin. Struct. Biol., 2004, vol. 14, pp. 273–282.
Li, Y., Bor, Y.-C., Misawa, Y., et al., An intron with a constitutive transport element is retained in a tap messenger RNA, Nature, 2006, vol. 443, pp. 234–237.
Lipshitz, H.D. and Smibert, C.A., Mechanisms of RNA localization and translational regulation, Curr. Opin. Genet. Devel., 2000, vol. 10, pp. 476–488.
Maniatis, T. and Tasic, B., Alternative pre-mRNA splicing and proteome expansion in metazoans, Nature, 2002, vol. 418, pp. 236–243.
Martin, K.C. and Ephrussi, A., MRNA localization: gene expression in the spatial dimension, Cell, 2009, vol. 136, pp. 719–730.
Matlin, A.J., Clark, F., and Smith, C.W., Understanding alternative splicing: towards a cellular code, Nat. Rev. Mol. Cell. Biol., 2005, vol. 6, pp. 386–398.
Mattick, J.S., Introns: evolution and function, Curr. Opin. Genet. Dev., 1994, vol. 4, pp. 823–831.
Mattick, J.S., Non-coding RNAs: the architects of eukaryotic complexity, EMBO Rep., 2001, vol. 21, pp. 986–991.
Mattick, J.S., RNA as the substrate for epigenome-environment interactions, BioEssays, 2010, vol. 32, pp. 548–552.
Mattick, J.S. and Gagen, M.J., The evolution of controlled multitasked gene networks: the role of introns and other noncoding RNAs in development of complex organisms, Mol. Biol. EV, 2001, vol. 18, pp. 1611–1630.
Meignin, C. and Davis, I., Transmitting the message: intracellular mRNA localization, Curr. Opin. Cell Biol., 2010, vol. 22, pp. 112–119.
Melhuish, T.A. and Wotton, D., The Tgif2 gene contains a retained intron within the coding sequence, BMC Mol. Biol., 2006, vol. 7, p. 2.
Michael, I.P., Kurlender, L., Memari, N., et al., Intron retention: a common splicing event within the human kallikrein gene family, Clin. Chem., 2005, vol. 51, pp. 506–515.
Mollet, I.G., Ben-Dov, C., Felicio-Silva, D., et al., Inconstrained mining of transcript data reveals increased alternative splicing complexity in the human transcriptome, Nucl. Acids Res., 2010, vol. 38, pp. 1–15.
Nilsen, T.W. and Graveley, B.R., Expansion of the eukaryotic proteome by alternative splicing, Nature, 2010, vol. 463, pp. 457–463.
Nott, A., Meislin, S.H., and Moore, M.J., A quantitative analysis of intron effects on mammalian gene expression, RNA, 2003, vol. 9, pp. 607–617.
Patthy, L., Genome evolution and the evolution of exonshuffling-a review, Gene, 1999, vol. 238, pp. 103–114.
Pesole, G., Mignone, F., Gissi, C., et al., Structural and functional features of eukaryotic mRNA untranslated regions, Gene, 2001, vol. 276, pp. 73–81.
Reznik, B. and Lykke-Andersen, J., Regulated and qualitycontrol mRNA turnover pathways in eukaryotes, Biochem. Soc. Trans., 2010, vol. 38, pp. 1506–1510.
Richter, J.D. and Lorenz, L.J., Selective translation of mRNAs at synapses, Curr. Opin. Neurobiol., 2002, vol. 12, pp. 300–304.
Sasaki, M., Takeda, E., and Takano, K., Molecular cloning and functional characterization of mouse Nxf family gene products, Genomics, 2005, vol. 85, pp. 641–653.
De Souza, S.J., Long, M., Schoenbach, L., et al., Intron positions correlate with module boundaries in ancient proteins, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 14632–14636.
Stamm, S., Ben-Ari, S., Rafalska, I., et al., Function of alternative splicing, Gene, 2005, vol. 344, pp. 1–20.
Wagner, E. and Lykke-Andersen, J., MRNA surveillance: the perfect persist, J. Cell Sci., 2002, vol. 115, pp. 3033–3038.
Wan, Y., Kertesz, M., Spitale, R.C., et al., Understanding the transcriptome through RNA structure, Natural Rev. Genetics, 2011, vol. 12, pp. 641–655.
White-Cooper, H., Molecular mechanisms of gene regulation during Drosophila spermatogenesis, Reproduction, 2010, vol. 139, pp. 11–21.
Wilusz, C.J. and Wilusz, J., Bringing the role of mRNA decay in the control of gene expression into focus, Trends Genet., 2004, vol. 20, pp. 491–497.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © L.A. Mamon, S.F. Kliver, A.O. Prosovskaya, V.R. Ginanova, Ye.V. Golubkova, 2013, published in Ekologicheskaya Genetika, 2013, Vol. 11, No. 3, pp. 3–13.
Rights and permissions
About this article
Cite this article
Mamon, L.A., Kliver, S.F., Prosovskaya, A.O. et al. The intron-containing transcript: an evolutionarily conserved characteristic of the genes orthologous to nxf1 (Nuclear Export Factor 1). Russ J Genet Appl Res 4, 434–443 (2014). https://doi.org/10.1134/S2079059714050104
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S2079059714050104