Evolution of Vault RNAs

Axel Mosig, Ruhr Universität Bochum, Bochum, Germany
Peter F Stadler, Santa Fe Institute, Santa Fe, New Mexico, USA

Published online: February 2011

DOI: 10.1002/9780470015902.a0022883

Vault ribonucleic acids (RNAs) are small, about 100 nt long, polymerase transcripts contained in the vault particles of eukaryotic cells. Although vaults are present in many but by no means all eukaryotes, an RNA component has been described in metazoa only. The RNAs exhibit conserved regions at the 3¢ and 5¢ ends containing also internal promoter elements. They form a panhandle-like well-conserved secondary structure. Most genomes contain only one or a small number of closely related vault RNA sequences. Only eutheria exhibit two clearly distinguished paralogues at syntenically conserved genomic locations. Their phylogenetic distribution is characterised by losses in major clades, whereas lophotrochozoa have vault particles and vault RNAs, and the entire system has been deleted in all ecdysozoa.

Key Concepts:

  • Vault RNA can be traced evolutionarily along with the vault particle and its key protein components, most notably MVP.
  • Vault RNA exhibits a concserved pan-handle secondary structure and expression patterns that are often mistaken as a microRNA.

Keywords: RNA secondary structure; animal genomes; polymerase III transcripts

Figure 1. The distribution of the MVP protein through the major eukaryotic clades shows that vaults are most likely ancient but have been lost many times. A black circle indicates clades in which MVP is found in most complete genomes or the available EST data. In green plants, MVP is present in many of the EST databases but so far is not contained in one of the assembled genomes.
Figure 2. Genomic locations of the two vault RNA loci. Triangle show the orientation in the genomic context, circles the presence of clear orthologues in the absence of clear linkage information.
Figure 3. Conserved elements associated with mammalian vtRNAs. The diagram, adapted from Stadler et al. (2009), shows patterns discovered by meme and indicates well-known pol-III upstream elements: distal sequence element, DSE; cyclic AMP response element CRE, which is a part of the larger proximal sequence element, PSE and the TATA box. The vtRNA genes themselves are delimited by conserved sequence patterns (5¢-side: motif 2 [blue] containing a Box A motif; 3¢-side: motifs 1 and 3 [cyan, red] containing the Box B motif and the pol-III terminator signal). Primate vtRNA-1 genes have a second copy of the Box B and terminator downstream of the experimentally determined end of the transcript. Mouse and rat vtRNA have an extended structure (Kickhoefer et al., 2003).
Figure 4. Expression of the computationally predicted vault RNAs is supported by short read sequencing data for both loci in Ciona intestinalis (Shi et al., 2009) and Schmidtea mediterranea (Friedländer et al., 2009; Lu et al., 2009).
Figure 5. Sequence and structure conservation in vtRNA (adapted from Stadler et al., 2009 and extended by lophotrochozoa vtRNA). (A) Lophotrochozoa (Schmidtea mediterrana, Helobdella robusta, Lottia gigantea, Echinococcus multilocularis, Capitella teleta, Aplysia californica, Hydra magnipapillata, Schicstosoma japonicum and Schistosoma mansoni). (B) basal deuterstomes, (C) teleosts, (D) shark (Callorhinchus milli) and sarcopterygii except eutheria, (E) eutherian vtRNA2 locus and (F) eutherian vtRNA1 (PCDH) locus. The upper panel shows the consensus secondary structures derived from (Stadler et al., 2009) extended by the newly discovered vtRNA sequences in lophotrochozoa described here. Although the essential hairpin in the secondary structure (circles in the secondary structure drawings indicating compensatory substitutions) and the box A motif (highlighted in blue) is well conserved in the lophotrochozoa vtRNA, the box B motif (highlighted in purple) appears lost in lophotrochozoa compared to all other known vtRNA genes.
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 References
    Abbondanza C, Rossi V, Roscigno A et al. (1998) Interaction of vault particles with estrogen receptor in the MCF-7 breast cancer cell. Journal of Cell Biology 141: 1301–1310.
    Anderson DH, Kickhoefer VA, Sievers SA, Rome LH and Eisenberg D (2007) Draft crystal structure of the vault shell at 9-Å resolution. PLoS Biology 5: e318.
    Berger W, Steiner E, Grusch M, Elbling L and Micksche M (2009) Vaults and the major vault protein: novel roles in signal pathway regulation and immunity. Cellular and Molecular Life Sciences 66: 43–61.
    Boria I, Gruber AR, Tanzer A et al. (2010) Nematode sbRNAs: homologs of vertebrate Y RNAs. Journal of Molecular Evolution 70: 346–358.
    Brameier M, Herwig A, Reinhardt R, Walter L and Gruber J (2010) Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs. Nucleic Acids Research Doi: 10.1093/nar/gkq776.
    Dickenson NE, Moore D, Suprenant KA and Dunn RC (2007) Vault ribonucleoprotein particles and the central mass of the nuclear pore complex. Photochemistry and Photobiology 83: 686–691.
    Ender C, Krek A, Friedländer MR et al. (2008) A human snoRNA with microRNA-like functions. Molecular Cell 32: 519–528.
    Friedländer MR, Adamidi C, Han T et al. (2009) High-resolution profiling and discovery of planarian small RNAs. Proceedings of the National Academy of Sciences of the USA 106: 11546–11551.
    Gopinath SC, Matsugami A, Katahira M and Kumar PK (2005) Human vault-associated non-coding RNAs bind to mitoxantrone, a chemotherapeutic compound. Nucleic Acids Research 33: 4874–4881.
    Gottesman MM, Fojo T and Bates SE (2002) Multidrug resistance in cancer: role of ATP-dependent transporters. Nature Reviews. Cancer 2: 48–58.
    Haussecker D, Huang Y, Lau A et al. (2010) Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA 16: 673–695.
    Izquierdo MA, Scheffer GL, Flens MJ et al. (1996) Major vault protein LRP-related multidrug resistance. European Journal of Cancer 32A: 979–984.
    Kato K, Tanaka H, Sumizawa T et al. (2008) A vault ribonucleoprotein particle exhibiting 39-fold dihedral symmetry. Acta Crystallographica. Section D, Biological Crystallography 64: 525–531.
    Kawaji H, Nakamura M, Takahashi1 Y et al. (2008) Hidden layers of human small RNAs. BMC Genomics 9: 157.
    Kedersha NL, Miquel MC, Bittner D and Rome LH (1990) Vaults. II. Ribonucleoprotein structures are highly conserved among higher and lower eukaryotes. Journal of Cell Biology 110: 895–901.
    Kickhoefer VA, Emre N, Stephen AG, Poderycki MJ and Rome LH (2003) Identification of conserved vault RNA expression elements and a non-expressed mouse vault RNA gene. Gene 309: 65–70.
    Kickhoefer VA, Searles RP, Kedersha NL et al. (1993) Vault ribonucleoprotein particles from rat and bullfrog contain a related small RNA that is transcribed by RNA polymerase III. Journal of Biological Chemistry 268: 7868–7873.
    Kloosterman WP, Steiner FA, Berezikov E et al. (2006) Cloning and expression of new microRNAs from zebrafish. Nucleic Acids Research 34: 2558–2569.
    Landgraf P, Rusu M, Sheridan R et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129: 1401–1414.
    Langenberger D, Bermudez-Santana C, Stadler PF and Hoffmann S (2010) Identification and classification of small RNAs in transcriptome sequence data. Pacific Symposium on Biocomputing 15: 80–87.
    Liang P, Wan Y, Yan Y et al. (2010) MVP interacts with YPEL4 and inhibits YPEL4-mediated activities of the ERK signal pathway. Biochemistry and Cell Biology 88: 445–450.
    Lu YC, Smielewska M, Palakodeti D et al. (2009) Deep sequencing identifies new and regulated microRNAs in Schmidtea mediterranea. RNA 15: 1483–1491.
    Mashima T, Kudo M, Takada Y et al. (2008) Interactions between antitumor drugs and vault RNA. Nucleic Acids Symposium Series (Oxford) 52: 217–218.
    Meiri E, Levy A, Benjamin H et al. (2010) Discovery of microRNAs and other small RNAs in solid tumors. Nucleic Acids Research 38(18) :6234–6246.
    book Mosig A, Chen JL and Stadler PF (2007a) "Homology search with fragmented nucleic acid sequence patterns". In: Giancarlo R and Hannenhalli S (eds) WABI 2007, Vol. 4645 of Lecture Notes in Computer Science, pp. 335–345. Berlin, Heidelberg: Springer.
    Mosig A, Guofeng M, Stadler BMR and Stadler PF (2007b) Evolution of the vertebrate Y RNA cluster. Theory in Bioscience 126: 9–14.
    Mrázek J, Kreutmayer SB, Grässer FA, Polacek N and Hüttenhofer A (2007) Subtractive hybridization identifies novel differentially expressed ncRNA species in EBV-infected human B cells. Nucleic Acids Research 35: e73.
    Nandy C, Mrázek J, Stoiber H et al. (2009) Epstein-Barr virus-induced expression of a novel human vault RNA. Journal of Molecular Biology 388: 776–784.
    Nawrocki EP, Kolbe DL and Eddy SR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25: 1335–1337.
    Perreault J, Perreault J-P and Boire G (2007) The Ro associated Y RNAs in metazoans: evolution and diversification. Molecular Biology and Evolution 24: 1678–1689.
    Persson H, Kvist A, Vallon-Christersson J et al. (2009) The non-coding RNA of the multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nature Cell Biology 11: 1268–1271.
    Poderycki MJ, Kickhoefer VA, Kaddis C S et al. (2006) The vault exterior shell is a dynamic structure that allows incorporation of vault-associated proteins into its interior. Biochemistry 45: 12184–12193.
    Rome L, Kedersha N and Chugani D (1991) Unlocking vaults: organelles in search of a function. Trends in Cell Biology 1: 47–50.
    Ryu SJ and Park SC (2009) Targeting major vault protein in senescence-associated apoptosis resistance. Expert Opinion on Therapeutic Targets 13: 479–484.
    Saraiya AA and Wang CC (2008) snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathogens 4: 11.
    Scheffer GL, Schroeijers AB, Izquierdo MA, Wiemer EA and Scheper RJ (2000) Lung resistance-related protein/major vault protein and vaults in multidrug-resistant cancer. Current Opinion in Oncology 12: 550–556.
    Shi W, Hendrix D, Levine M and Haley B (2009) A distinct class of small RNAs arises from pre-miRNA-proximal regions in a simple chordate. Nature Structural & Molecular Biology 16: 183–189.
    Smith S (2001) The world according to PARP. Trends in Biochemical Sciences 26: 174–179.
    Stadler PF, Chen JJ-L, Hackermüller J et al. (2009) Evolution of vault RNAs. Molecular Biology and Evolution 26: 1975–1991.
    Steiner E, Holzmann K, Elbling L, Micksche M and Berger W (2006) Cellular functions of vaults and their involvement in multidrug resistance. Current Drug Targets 7: 923–934.
    Stewart PL, Makabi M, Lang J et al. (2005) Sea urchin vault structure, composition, and differential localization during development. BMC Developmental Biology 5: 3.
    Suprenant KA, Bloom N, Fang J and Lushington G (2007) The major vault protein is related to the toxic anion resistance protein (TelA) family. Journal of Experimental Biology 210: 946–955.
    Taft RJ, Glazov EA, Lassmann T et al. (2009) Small RNAs derived from snoRNAs. RNA 15: 1233–1240.
    Tanaka H, Kato K, Yamashita E et al. (2009) The structure of rat liver vault at 3.5 Å resolution. Science 323: 384–388.
    Vasu SK and Rome LH (1995) Dictyostelium vaults: disruption of the major proteins reveals growth and morphological defects and uncovers a new associated protein. Journal of Biological Chemistry 270: 16588–16594.
    Vilalta A, Kickhoefer VA, Rome LH and Johnson DL (1994) The rat vault RNA gene contains a unique RNA polymerase III promoter composed of both external and internal elements that function synergistically. Journal of Biological Chemistry 269: 29752–29759.
    Zhang Y, Wang J, Huang S et al. (2009) Systematic identification and characterization of chicken (Gallus gallus) ncRNAs, Nucl. Nucleic Acids Research 37: 6562–6574.
    van Zon A, Mossink MH, Houtsmuller A B et al. (2006) Vault mobility depends in part on microtubules and vaults can be recruited to the nuclear envelope. Experimental Cell Research 312: 245–255.
    van Zon A, Mossink MH, Scheper RJ, Sonneveld P and Wiemer EAC (2003) The vault complex. Cellular and Molecular Life Sciences 60: 1828–1837.
    van Zon A, Mossink MH, Schoester M et al. (2001) Multiple human vault RNAs. Journal of Biological Chemistry 276: 37715–37721.
 Further Reading
    Athanasius F, Backofen R, Bernhart S et al. (2007) RNAs everywhere: genome-wide annotation of structured RNAs. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution 308(1): 1.
    Bompfünewerer A, Flamm C, Fried C et al. (2005) Evolutionary patterns of non-coding RNAs. Theory in Biosciences 123(4): 301–369.

Related Sub-Topics:

Cell Compartments and Cellular Organelles | Molecular Evolution | RNA Structure and Function | Noncoding RNA | Evolution of Coding and Functional Modules
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Article Title: Evolution of Vault RNAs
 
How to Cite close
Mosig, Axel, and Stadler, Peter F(Feb 2011) Evolution of Vault RNAs. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022883]