Abstract
Non-coding (nc)RNAs have recently emerged as ubiquitous and important regulators of a multitude of different processes, such as stress response, cell differentiation, infection, and cell death. The means by which ncRNAs affect these processes are numerous and diverse, ranging from protein localization to regulation of gene expression. ncRNA-mediated gene expression control has been the subject of especially intense study in recent years and has shown to occur through several mechanisms. Different ncRNAs can regulate gene expression transcriptionally by inducing modification of DNA or chromatin, or post-transcriptionally by directing cleavage, degradation, or translational inhibition of messenger (m)RNAs. ncRNAs come in a broad spectrum of sizes, from ~20 nucleotides (nt) to several thousand nt, and function in complexes with various proteins that usually exert a catalytic function while the RNAs act as guides. In Dictyostelia, we have only started to understand the extent of ncRNA regulation, mostly from studies in Dictyostelium discoideum, which is the focus of this chapter.
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References
Andersen ES, Rosenblad MA, Larsen N, Westergaard JC, Burks J, Wower IK, Wower J, Gorodkin J, Samuelsson T, Zwieb C (2006) The tmRDB and SRPDB resources. Nucleic Acids Res 34 (Database issue):D163–168. doi:10.1093/nar/gkj142
Anderson JT (2005) RNA turnover: unexpected consequences of being tailed. Curr Biol 15(16):R635–638. doi:10.1016/j.cub.2005.08.002
Aspegren A, Hinas A, Larsson P, Larsson A, Soderbom F (2004) Novel non-coding RNAs in Dictyostelium discoideum and their expression during development. Nucleic Acids Res 32(15):4646–4656. doi:10.1093/nar/gkh804
Avesson L, Reimegård J, Wagner EG, Söderbom F (2012) MicroRNAs in Amoebozoa: deep sequencing of the small RNA population in the social amoeba Dictyostelium discoideum reveals developmentally regulated microRNAs. RNA 18(10):1771-1781. doi:10.1261/rna.033175.112
Avesson L, Schumacher HT, Fechter P, Romby P, Hellman U, Söderbom F (2011) Abundant class of non-coding RNA regulates development in the social amoeba Dictyostelium discoideum. RNA Biol 8(6):1094-1104. doi:10.4161/rna.8.6.17214
Birney E, Stamatoyannopoulos JA, Dutta A et al (2007) Identification and analysis of functional elements in 1 % of the human genome by the ENCODE pilot project. Nature 447(7146):799–816. doi:10.1038/nature05874
Boesler C, Kruse J, Soderbom F, Hammann C (2011) Sequence and generation of mature ribosomal RNA transcripts in Dictyostelium discoideum. J Biol Chem 286(20):17693–17703. doi:10.1074/jbc.M110.208306, M110.208306 [pii]
Braun L, Cannella D, Ortet P, Barakat M, Sautel CF, Kieffer S, Garin J, Bastien O, Voinnet O, Hakimi MA (2010) A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii. PLoS Pathog 6(5):e1000920. doi:10.1371/journal.ppat.1000920
Bullerwell CE, Burger G, Gott JM, Kourennaia O, Schnare MN, Gray MW (2010) Abundant 5S rRNA-like transcripts encoded by the mitochondrial genome in amoebozoa. Eukaryot Cell 9(5):762–773. doi:10.1128/ec.00013-10
Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136(4):642–655. doi:10.1016/j.cell.2009.01.035 ,S0092-8674(09)00083-X [pii]
Cerutti H, Casas-Mollano J (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 50(2):81–99. doi:10.1007/s00294-006-0078-x
Clark MB, Mattick JS (2011) Long noncoding RNAs in cell biology. Semin Cell Dev Biol. doi:10.1016/j.semcdb.2011.01.001, S1084-9521(11)00013-9 [pii]
Clery A, Blatter M, Allain FH (2008) RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 18(3):290–298. doi:10.1016/j.sbi.2008.04.002, S0959-440X(08)00058-4 [pii]
Czech B, Hannon GJ (2011) Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet 12(1):19–31. doi:10.1038/nrg2916, nrg2916 [pii]
Darzacq X, Kiss T (2000) Processing of intron-encoded box C/D small nucleolar RNAs lacking a 5′,3′-terminal stem structure. Mol Cell Biol 20(13):4522–4531
Dieci G, Fiorino G, Castelnuovo M, Teichmann M, Pagano A (2007) The expanding RNA polymerase III transcriptome. Trends Genet 23(12):614–622. doi:10.1016/j.tig.2007.09.001
Dieci G, Preti M, Montanini B (2009) Eukaryotic snoRNAs: a paradigm for gene expression flexibility. Genomics 94(2):83–88. doi:10.1016/j.ygeno.2009.05.002
Dubin M, Fuchs J, Graf R, Schubert I, Nellen W (2010) Dynamics of a novel centromeric histone variant CenH3 reveals the evolutionary ancestral timing of centromere biogenesis. Nucleic Acids Res. doi:10.1093/nar/gkq664, gkq664 [pii]
Ellis JC, Brown DD, Brown JW (2010) The small nucleolar ribonucleoprotein (snoRNP) database. RNA 16(4):664–666. doi:10.1261/rna.1871310
Ender C, Krek A, Friedlander MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G (2008) A human snoRNA with microRNA-like functions. Mol Cell 32(4):519–528. doi:10.1016/j.molcel.2008.10.017, S1097-2765(08)00733-8 [pii]
Esakova O, Krasilnikov AS (2010) Of proteins and RNA: the RNase P/MRP family. RNA 16(9):1725–1747. doi:10.1261/rna.2214510
Esteller M (2011) Non-coding RNAs in human disease. Nat Rev Genet 12(12):861–874
Farbrother P, Wagner C, Na J, Tunggal B, Morio T, Urushihara H, Tanaka Y, Schleicher M, Steinert M, Eichinger L (2006) Dictyostelium transcriptional host cell response upon infection with Legionella. Cell Microbiol 8(3):438–456. doi:10.1111/j.1462-5822.2005.00633.x, CMI633 [pii]
Fischer U, Englbrecht C, Chari A (2011) Biogenesis of spliceosomal small nuclear ribonucleoproteins. Wiley Interdiscip Rev RNA 2(5):718–731. doi:10.1002/wrna.87
Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92–105. doi:10.1101/gr.082701.108
Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10(2):94–108. doi:10.1038/nrg2504
Glockner G, Heidel AJ (2009) Centromere sequence and dynamics in Dictyostelium discoideum. Nucleic Acids Res 37(6):1809–1816. doi:10.1093/nar/gkp017, gkp017 [pii]
Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35(3 Pt 2):849–857
Heidel A, Lawal H, Felder M, Schilde C, Helps N, Tunggal B, Rivero F, John U, Schleicher M, Eichinger L, Platzer M, Noegel A, Schaap P, Glöckner G (2011) Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication. Genome Res 21(11):1882–1891. doi:10.1101/gr.121137.111
Hildebrandt M, Nellen W (1992) Differential antisense transcription from the Dictyostelium EB4 gene locus: implications on antisense-mediated regulation of mRNA stability. Cell 69(1):197–204, 0092-8674(92)90130-5 [pii]
Hinas A, Larsson P, Avesson L, Kirsebom LA, Virtanen A, Soderbom F (2006) Identification of the major spliceosomal RNAs in Dictyostelium discoideum reveals developmentally regulated U2 variants and polyadenylated snRNAs. Eukaryot Cell 5(6):924–934. doi:10.1128/ec.00065-06
Hinas A, Reimegard J, Wagner EG, Nellen W, Ambros VR, Soderbom F (2007) The small RNA repertoire of Dictyostelium discoideum and its regulation by components of the RNAi pathway. Nucleic Acids Res 35(20):6714–6726. doi:10.1093/nar/gkm707, gkm707 [pii]
Hinas A, Soderbom F (2007) Treasure hunt in an amoeba: non-coding RNAs in Dictyostelium discoideum. Curr Genet 51(3):141–159. doi:10.1007/s00294-006-0112-z
Hogg JR, Collins K (2008) Structured non-coding RNAs and the RNP renaissance. Curr Opin Chem Biol 12(6):684–689. doi:10.1016/j.cbpa.2008.09.027
International Human Genome Sequencing Consortium (2004) Finishing the euchromatic sequence of the human genome. Nature 431(7011):931–945. doi:10.1038/nature03001
Jochl C, Rederstorff M, Hertel J, Stadler PF, Hofacker IL, Schrettl M, Haas H, Huttenhofer A (2008) Small ncRNA transcriptome analysis from Aspergillus fumigatus suggests a novel mechanism for regulation of protein synthesis. Nucleic Acids Res 36(8):2677–2689. doi:10.1093/nar/gkn123
Kalavrizioti D, Vourekas A, Drainas D (2007) DRpp 20 and DRpp40: two protein subunits involved in Dictyostelium discoideum ribonuclease P holoenzyme assembly. Gene 400(1–2):52–59. doi:10.1016/j.gene.2007.05.020
Kaneda S, Gotoh O, Seno T, Takeishi K (1983) Nucleotide sequence of Dictyostelium small nuclear RNA Dd8 not homologous to any other sequenced small nuclear RNA. J Biol Chem 258(17):10606–10613
Kikovska E, Svard SG, Kirsebom LA (2007) Eukaryotic RNase P RNA mediates cleavage in the absence of protein. Proc Natl Acad Sci USA 104(7):2062–2067. doi:10.1073/pnas.0607326104
Kishore S, Khanna A, Zhang Z, Hui J, Balwierz PJ, Stefan M, Beach C, Nicholls RD, Zavolan M, Stamm S (2010) The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing. Hum Mol Genet 19(7):1153–1164. doi:10.1093/hmg/ddp585
Kishore S, Stamm S (2006) The snoRNA HBII-52 regulates alternative splicing of the serotonin receptor 2C. Science 311(5758):230–232. doi:10.1126/science.1118265
Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39(suppl 1):D152–D157. doi:10.1093/nar/gkq1027
Krol J, Loedige I, Filipowicz W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 11(9):597–610. doi:10.1038/nrg2843
Kuhlmann M, Borisova BE, Kaller M, Larsson P, Stach D, Na J, Eichinger L, Lyko F, Ambros V, Soderbom F, Hammann C, Nellen W (2005) Silencing of retrotransposons in Dictyostelium by DNA methylation and RNAi. Nucleic Acids Res 33(19):6405–6417. doi:10.1093/nar/gki952, 33/19/6405 [pii]
Kumimoto H, Yoshida H, Okamoto K (1995) RNA polymerase II transcribes Dictyostelium untranslatable gene, dutA, specifically in the developmental phase. Biochem Biophys Res Commun 216(1):273–278. doi:10.1006/bbrc.1995.2620
Larsson P, Hinas A, Ardell DH, Kirsebom LA, Virtanen A, Soderbom F (2008) De novo search for non-coding RNA genes in the AT-rich genome of Dictyostelium discoideum: performance of Markov-dependent genome feature scoring. Genome Res 18(6):888–899. doi:10.1101/gr.069104.107, gr.069104.107 [pii]
Lee JT (2010) The X as model for RNA’s Niche in epigenomic regulation. Cold Spring Harb Perspect Biol 2(9):a003749 doi:10.1101/cshperspect.a003749
Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115(7):787–798
Liang XH, Uliel S, Hury A, Barth S, Doniger T, Unger R, Michaeli S (2005) A genome-wide analysis of C/D and H/ACA-like small nucleolar RNAs in Trypanosoma brucei reveals a trypanosome-specific pattern of rRNA modification. RNA 11(5):619–645. doi:10.1261/rna.7174805
MacRae IJ, Doudna JA (2007) Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Curr Opin Struct Biol 17(1):138–145. doi:10.1016/j.sbi.2006.12.002, S0959-440X(06)00212-0 [pii]
Maeda M, Sakamoto H, Iranfar N, Fuller D, Maruo T, Ogihara S, Morio T, Urushihara H, Tanaka Y, Loomis WF (2003) Changing patterns of gene expression in dictyostelium prestalk cell subtypes recognized by in situ hybridization with genes from microarray analyses. Eukaryot Cell 2(3):627–637
Maida Y, Masutomi K (2011) RNA-dependent RNA polymerases in RNA silencing. Biol Chem 392(4):299–304. doi:10.1515/BC.2011.035
Marquez SM, Harris JK, Kelley ST, Brown JW, Dawson SC, Roberts EC, Pace NR (2005) Structural implications of novel diversity in eucaryal RNase P RNA. RNA 11(5):739–751. doi:10.1261/rna.7211705
Martens H, Novotny J, Oberstrass J, Steck TL, Postlethwait P, Nellen W (2002) RNAi in Dictyostelium: the role of RNA-directed RNA polymerases and double-stranded RNase. Mol Biol Cell 13(2):445–453. doi:10.1091/mbc.01-04-0211
Maruo T, Sakamoto H, Iranfar N, Fuller D, Morio T, Urushihara H, Tanaka Y, Maeda M, Loomis WF (2004) Control of cell type proportioning in Dictyostelium discoideum by differentiation-inducing factor as determined by in situ hybridization. Eukaryot Cell 3(5):1241–1248. doi:10.1128/ec.3.5.1241-1248.2004
Mattick JS (2009) The genetic signatures of noncoding RNAs. PLoS Genet 5(4):e1000459. doi:10.1371/journal.pgen.1000459
Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10(3):155–159. doi:10.1038/nrg2521, nrg2521 [pii]
Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447(7148):1126–1129. http://www.nature.com/nature/journal/v447/n7148/suppinfo/nature05903_S1.html
Okafuji T, Abe F, Maeda Y (1997) Antisense-mediated regulation of Annexin VII gene expression during the transition from growth to differentiation in Dictyostelium discoideum. Gene 189(1):49–56
Pannucci JA, Haas ES, Hall TA, Harris JK, Brown JW (1999) RNase P RNAs from some Archaea are catalytically active. Proc Natl Acad Sci USA 96(14):7803–7808
Pi M, Morio T, Urushihara H, Tanaka Y (1998) Characterization of a novel small RNA encoded by Dictyostelium discoideum mitochondrial DNA. Mol Gen Genet 257(2):124–131
Piccinelli P, Rosenblad MA, Samuelsson T (2005) Identification and analysis of ribonuclease P and MRP RNA in a broad range of eukaryotes. Nucleic Acids Res 33(14):4485–4495. doi:10.1093/nar/gki756
Pool MR (2005) Signal recognition particles in chloroplasts, bacteria, yeast and mammals (review). Mol Membr Biol 22(1–2):3–15
Popova B, Kuhlmann M, Hinas A, Soderbom F, Nellen W (2006) HelF, a putative RNA helicase acts as a nuclear suppressor of RNAi but not antisense mediated gene silencing. Nucleic Acids Res 34(3):773–784. doi:10.1093/nar/gkj465, 34/3/773 [pii]
Reichow SL, Hamma T, Ferré-D’Amaré AR, Varani G (2007) The structure and function of small nucleolar ribonucleoproteins. Nucleic Acids Res 35(5):1452–1464. doi:10.1093/nar/gkl1172
Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520
Rodriguez-Trelles F, Tarrio R, Ayala FJ (2006) Origins and evolution of spliceosomal introns. Annu Rev Genet 40:47–76. doi:10.1146/annurev.genet.40.110405.090625
Rosenblad MA, Zwieb C, Samuelsson T (2004) Identification and comparative analysis of components from the signal recognition particle in protozoa and fungi. BMC Genomics 5(1):5. doi:10.1186/1471-2164-5-5
Russell AG, Schnare MN, Gray MW (2006) A large collection of compact box C/D snoRNAs and their isoforms in Euglena gracilis: structural, functional and evolutionary insights. J Mol Biol 357(5):1548–1565. doi:10.1016/j.jmb.2006.01.063
Saraiya AA, Wang CC (2008) snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4(11):e1000224. doi:10.1371/journal.ppat.1000224
Shimada N, Kawata T (2007) Evidence that noncoding RNA dutA is a multicopy suppressor of Dictyostelium discoideum STAT protein Dd-STATa. Eukaryot Cell 6(6):1030–1040. doi:10.1128/ec.00035-07
Stamatopoulou V, Toumpeki C, Tzakos A, Vourekas A, Drainas D (2010) Domain architecture of the DRpp 29 protein and its interaction with the RNA subunit of Dictyostelium discoideum RNase P. Biochemistry 49(50):10714–10727. doi:10.1021/bi101297z
Stathopoulos C, Kalpaxis DL, Drainas D (1995) Partial purification and characterization of RNase P from Dictyostelium discoideum. Eur J Biochem 228(3):976–980
Sucgang R, Kuo A, Tian X et al (2011) Comparative genomics of the social amoebae Dictyostelium discoideum and Dictyostelium purpureum. Genome Biol 12(2):R20
Takeishi K, Kaneda S (1981) Isolation and characterization of small nuclear RNAs from Dictyostelium discoideum. J Biochem 90(2):299–308
Vitali P, Basyuk E, Le Meur E, Bertrand E, Muscatelli F, Cavaille J, Huttenhofer A (2005) ADAR2-mediated editing of RNA substrates in the nucleolus is inhibited by C/D small nucleolar RNAs. J Cell Biol 169(5):745–753. doi:10.1083/jcb.200411129
Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687. doi:10.1016/j.cell.2009.01.046, S0092-8674(09)00128-7 [pii]
Vourekas A, Kalavrizioti D, Zarkadis IK, Spyroulias GA, Stathopoulos C, Drainas D (2007) A 40.7 kDa Rpp 30/Rpp1 homologue is a protein subunit of Dictyostelium discoideum RNase P holoenzyme. Biochimie 89(3):301–310. doi:10.1016/j.biochi.2006.11.006
Wahl MC, Will CL, Luhrmann R (2009) The spliceosome: design principles of a dynamic RNP machine. Cell 136(4):701–718. doi:10.1016/j.cell.2009.02.009, S0092-8674(09)00146-9 [pii]
Watanabe T, Miyashita K, Saito TT, Nabeshima K, Nojima H (2002) Abundant poly(A)-bearing RNAs that lack open reading frames in Schizosaccharomyces pombe. DNA Res 9(6):209–215
Whitney TJ, Gardner DG, Mott ML, Brandon M (2010) Identifying the molecular basis of functions in the transcriptome of the social amoeba Dictyostelium discoideum. Genet Mol Res 9(1):394–415. doi:10.4238/vol9-1gmr752
Wilusz JE, Sunwoo H, Spector DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23(13):1494–1504. doi:10.1101/gad.1800909, 23/13/1494 [pii]
Win TZ, Draper S, Read RL, Pearce J, Norbury CJ, Wang SW (2006) Requirement of fission yeast Cid14 in polyadenylation of rRNAs. Mol Cell Biol 26(5):1710–1721. doi:10.1128/MCB.26.5.1710-1721.2006, 26/5/1710 [pii]
Wise JA, Weiner AM (1981) The small nuclear RNAs of the cellular slime mold Dictyostelium discoideum. Isolation and characterization. J Biol Chem 256(2):956–963
Yoshida H, Kumimoto H, Okamoto K (1994) dutA RNA functions as an untranslatable RNA in the development of Dictyostelium discoideum. Nucleic Acids Res 22(1):41–46. doi:10.1093/nar/22.1.41
Yu B, Fey P, Kestin-Pilcher KE, Fedorov A, Prakash A, Chisholm RL, Wu JY (2011) Spliceosomal genes in the D. discoideum genome: a comparison with those in H. sapiens, D. melanogaster, A. thaliana and S. cerevisiae. Protein Cell 2(5):395–409. doi:10.1007/s13238-011-1052-z
Zhao T, Li G, Mi S, Li S, Hannon GJ, Wang X-J, Qi Y (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21(10):1190–1203. doi:10.1101/gad.1543507
Acknowledgments
We thank present and former members of the laboratory for experimental input and helpful discussions. This work was supported by The Swedish Research Council (to F.S. and to Uppsala RNA Research Center), The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS), and the European Community (FOSRAK, EC005120).
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Avesson, L., Hinas, A., Söderbom, F. (2013). Non-coding RNAs in Dictyostelium discoideum and Other Dictyostelid Social Amoebae. In: Romeralo, M., Baldauf, S., Escalante, R. (eds) Dictyostelids. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-38487-5_6
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