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MicroRNA Pathways in Drosophila

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From Nucleic Acids Sequences to Molecular Medicine

Part of the book series: RNA Technologies ((RNATECHN))

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Abstract

MicroRNAs belong to a class of 20–25 nucleotide noncoding RNAs that posttranscriptionally regulate gene expression in a sequence-specific manner. Members of the microRNA family play roles in the normal physiology and development of diverse organisms. In this review, we focus on the recent progress made in understanding the roles of microRNAs in Drosophila biology. The topics discussed include biogenesis, discovery, mechanism of action, and function of microRNAs in diverse aspects of fly development.

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References

  • Aravin AA, Lagos-Quintana M, Yalcin A et al (2003) The small RNA profile during Drosophila melanogaster development. Dev Cell 5:337–350

    Article  PubMed  CAS  Google Scholar 

  • Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    Article  PubMed  CAS  Google Scholar 

  • Bejarano F, Smibert P, Lai EC (2010) miR-9a prevents apoptosis during wing development by repressing Drosophila LIM-only. Dev Biol 338:63–73

    Article  PubMed  CAS  Google Scholar 

  • Bentwich I (2005) Prediction and validation of microRNAs and their targets. FEBS Lett 579:5904–5910

    Article  PubMed  CAS  Google Scholar 

  • Berezikov E, Robine N, Samsonova A et al (2010) Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence. Genome Res 21:203–215

    Article  PubMed  Google Scholar 

  • Biryukova I, Asmar J, Abdesselem H et al (2009) Drosophila mir-9a regulates wing development via fine-tuning expression of the LIM only factor, dLMO. Dev Biol 327:487–496

    Article  PubMed  CAS  Google Scholar 

  • Brennecke J, Hipfner DR, Stark A et al (2003) Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113:25–36

    Article  PubMed  CAS  Google Scholar 

  • Brennecke J, Stark A, Russell RB et al (2005) Principles of microRNA-target recognition. PLoS Biol 3:e85

    Article  PubMed  Google Scholar 

  • Caygill EE, Johnston LA (2008) Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Curr Biol 18:943–950

    Article  PubMed  CAS  Google Scholar 

  • Cayirlioglu P, Kadow IG, Zhan X et al (2008) Hybrid neurons in a microRNA mutant are putative evolutionary intermediates in insect CO2 sensory systems. Science 319:1256–1260

    Article  PubMed  CAS  Google Scholar 

  • Cohen SM, Brennecke J, Stark A (2006) Denoising feedback loops by thresholding—a new role for microRNAs. Genes Dev 20:2769–2772

    Article  PubMed  CAS  Google Scholar 

  • Enright AJ, John B, Gaul U et al (2003) MicroRNA targets in Drosophila. Genome Biol 5:R1

    Article  PubMed  Google Scholar 

  • Fabian MR, Sonenberg N, Filipowicz W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79:351–379

    Article  PubMed  CAS  Google Scholar 

  • Forstemann K, Horwich MD, Wee L et al (2007) Drosophila microRNAs are sorted into functionally distinct argonaute complexes after production by dicer-1. Cell 130:287–297

    Article  PubMed  Google Scholar 

  • Griffiths-Jones S (2004) The microRNA registry. Nucleic Acids Res 32(Database issue):D109–D111

    Article  PubMed  CAS  Google Scholar 

  • Grun D, Wang YL, Langenberger D et al (2005) MicroRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput Biol 1:e13

    Article  PubMed  Google Scholar 

  • Herranz H, Cohen SM (2010) MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev 24:1339–1344

    Article  PubMed  CAS  Google Scholar 

  • Hilgers V, Bushati N, Cohen SM (2010) Drosophila microRNAs 263a/b confer robustness during development by protecting nascent sense organs from apoptosis. PLoS Biol 8:e1000396

    Article  PubMed  Google Scholar 

  • Hipfner DR, Weigmann K, Cohen SM (2002) The bantam gene regulates Drosophila growth. Genetics 161:1527–1537

    PubMed  CAS  Google Scholar 

  • Hobert O (2004) Common logic of transcription factor and microRNA action. Trends Biochem Sci 29:462–468

    Article  PubMed  CAS  Google Scholar 

  • Hyun S, Lee JH, Jin H et al (2009) Conserved microRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 139:1096–1108

    Article  PubMed  CAS  Google Scholar 

  • Iovino N, Pane A, Gaul U (2009) miR-184 has multiple roles in Drosophila female germline development. Dev Cell 17:123–133

    Article  PubMed  CAS  Google Scholar 

  • Ishizuka A, Siomi MC, Siomi H (2002) A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev 16:2497–2508

    Article  PubMed  CAS  Google Scholar 

  • Jiang F, Ye X, Liu X et al (2005) Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes Dev 19:1674–1679

    Article  PubMed  CAS  Google Scholar 

  • Kadener S, Menet JS, Sugino K et al (2009) A role for microRNAs in the Drosophila circadian clock. Genes Dev 23:2179–2191

    Article  PubMed  CAS  Google Scholar 

  • Karres JS, Hilgers V, Carrera I et al (2007) The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell 131:136–145

    Article  PubMed  CAS  Google Scholar 

  • Kawamata T, Tomari Y (2010) Making RISC. Trends Biochem Sci 35:368–376

    Article  PubMed  CAS  Google Scholar 

  • Kennell JA, Gerin I, MacDougald OA et al (2008) The microRNA miR-8 is a conserved negative regulator of Wnt signaling. Proc Natl Acad Sci USA 105:15417–15422

    Article  PubMed  CAS  Google Scholar 

  • Kertesz M, Iovino N, Unnerstall U et al (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39:1278–1284

    Article  PubMed  CAS  Google Scholar 

  • Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10:126–139

    Article  PubMed  CAS  Google Scholar 

  • Krek A, Grun D, Poy MN et al (2005) Combinatorial microRNA target predictions. Nat Genet 37:495–500

    Article  PubMed  CAS  Google Scholar 

  • Kwon C, Han Z, Olson EN et al (2005) MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. Proc Natl Acad Sci USA 102:18986–18991

    Article  PubMed  CAS  Google Scholar 

  • Lagos-Quintana M, Rauhut R, Lendeckel W et al (2001) Identification of novel genes coding for small expressed RNAs. Science 294:853–858

    Article  PubMed  CAS  Google Scholar 

  • Lai EC (2002) Micro RNAs are complementary to 3′UTR sequence motifs that mediate negative post-transcriptional regulation. Nat Genet 30:363–364

    Article  PubMed  CAS  Google Scholar 

  • Lai EC, Posakony JW (1997) The bearded box, a novel 3′UTR sequence motif, mediates negative post-transcriptional regulation of bearded and enhancer of split complex gene expression. Development 124:4847–4856

    PubMed  CAS  Google Scholar 

  • Lai EC, Tam B, Rubin GM (2005) Pervasive regulation of Drosophila Notch target genes by GY-box-, Brd-box-, and K-box-class microRNAs. Genes Dev 19:1067–1080

    Article  PubMed  CAS  Google Scholar 

  • Lai EC, Tomancak P, Williams RW et al (2003) Computational identification of Drosophila microRNA genes. Genome Biol 4:R42

    Article  PubMed  Google Scholar 

  • Lau NC, Lim LP, Weinstein EG et al (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858–862

    Article  PubMed  CAS  Google Scholar 

  • Leaman D, Chen PY, Fak J et al (2005) Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development. Cell 121:1097–1108

    Article  PubMed  CAS  Google Scholar 

  • Lee RC, Ambros V (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294:862–864

    Article  PubMed  CAS  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Ahn C, Han J et al (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415–419

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Jeon K, Lee JT et al (2002) MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 21:4663–4670

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Kim M, Han J et al (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–4060

    Article  PubMed  CAS  Google Scholar 

  • Li X, Carthew RW (2005) A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123:1267–1277

    Article  PubMed  CAS  Google Scholar 

  • Li X, Cassidy JJ, Reinke CA et al (2009) A microRNA imparts robustness against environmental fluctuation during development. Cell 137:273–282

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Wang F, Lee JA et al (2006) MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Genes Dev 20:2793–2805

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Rand TA, Kalidas S et al (2003) R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301:1921–1925

    Article  PubMed  CAS  Google Scholar 

  • Long D, Lee R, Williams P et al (2007) Potent effect of target structure on microRNA function. Nat Struct Mol Biol 14:287–294

    Article  PubMed  CAS  Google Scholar 

  • Loya CM, Lu CS, Van Vactor D et al (2009) Transgenic microRNA inhibition with spatiotemporal specificity in intact organisms. Nat Methods 6:897–903

    Article  PubMed  CAS  Google Scholar 

  • Min H, Yoon S (2010) Got target? Computational methods for microRNA target prediction and their extension. Exp Mol Med 42:233–244

    Article  PubMed  CAS  Google Scholar 

  • Nguyen HT, Frasch M (2006) MicroRNAs in muscle differentiation: lessons from Drosophila and beyond. Curr Opin Genet Dev 16:533–539

    Article  PubMed  CAS  Google Scholar 

  • Nolo R, Morrison CM, Tao C et al (2006) The bantam microRNA is a target of the hippo tumor-suppressor pathway. Curr Biol 16:1895–1904

    Article  PubMed  CAS  Google Scholar 

  • Okamura K, Hagen JW, Duan H et al (2007) The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130:89–100

    Article  PubMed  CAS  Google Scholar 

  • Park JE, Heo I, Tian Y et al (2011) Dicer recognizes the 5′end of RNA for efficient and accurate processing. Nature 475:201–205

    Article  PubMed  CAS  Google Scholar 

  • Parrish JZ, Xu P, Kim CC et al (2009) The microRNA bantam functions in epithelial cells to regulate scaling growth of dendrite arbors in Drosophila sensory neurons. Neuron 63:788–802

    Article  PubMed  CAS  Google Scholar 

  • Pasquinelli AE, Reinhart BJ, Slack F et al (2000) Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408:86–89

    Article  PubMed  CAS  Google Scholar 

  • Pek JW, Lim AK, Kai T (2009) Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev Cell 17:417–424

    Article  PubMed  CAS  Google Scholar 

  • Reinhart BJ, Slack FJ, Basson M et al (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901–906

    Article  PubMed  CAS  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW et al (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    Article  PubMed  CAS  Google Scholar 

  • Ronshaugen M, Biemar F, Piel J et al (2005) The Drosophila microRNA iab-4 causes a dominant homeotic transformation of halteres to wings. Genes Dev 19:2947–2952

    Article  PubMed  CAS  Google Scholar 

  • Ruby JG, Stark A, Johnston WK et al (2007) Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 17:1850–1864

    Article  PubMed  CAS  Google Scholar 

  • Rybak A, Fuchs H, Smirnova L et al (2008) A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 10:987–993

    Article  PubMed  CAS  Google Scholar 

  • Saito K, Ishizuka A, Siomi H et al (2005) Processing of pre-microRNAs by the Dicer-1-Loquacious complex in Drosophila cells. PLoS Biol 3:e235

    Article  PubMed  Google Scholar 

  • Sempere LF, Sokol NS, Dubrovsky EB et al (2003) Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-complex gene activity. Dev Biol 259:9–18

    Article  PubMed  CAS  Google Scholar 

  • Silver SJ, Hagen JW, Okamura K et al (2007) Functional screening identifies miR-315 as a potent activator of Wingless signaling. Proc Natl Acad Sci USA 104:18151–18156

    Article  PubMed  CAS  Google Scholar 

  • Siomi H, Siomi MC (2010) Posttranscriptional regulation of microRNA biogenesis in animals. Mol Cell 38:323–332

    Article  PubMed  CAS  Google Scholar 

  • Sokol NS, Ambros V (2005) Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. Genes Dev 19:2343–2354

    Article  PubMed  CAS  Google Scholar 

  • Sokol NS, Xu P, Jan YN et al (2008) Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes Dev 22:1591–1596

    Article  PubMed  CAS  Google Scholar 

  • Stark A, Brennecke J, Bushati N et al (2005) Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3′UTR evolution. Cell 123:1133–1146

    Article  PubMed  CAS  Google Scholar 

  • Stark A, Brennecke J, Russell RB et al (2003) Identification of Drosophila microRNA targets. PLoS Biol 1:E60

    Article  PubMed  Google Scholar 

  • Stark A, Bushati N, Jan CH et al (2008) A single Hox locus in Drosophila produces functional microRNAs from opposite DNA strands. Genes Dev 22:8–13

    Article  PubMed  CAS  Google Scholar 

  • Stark A, Kheradpour P, Parts L et al (2007) Systematic discovery and characterization of fly microRNAs using 12 Drosophila genomes. Genome Res 17:1865–1879

    Article  PubMed  CAS  Google Scholar 

  • Teleman AA, Maitra S, Cohen SM (2006) Drosophila lacking microRNA miR-278 are defective in energy homeostasis. Genes Dev 20:417–422

    Article  PubMed  CAS  Google Scholar 

  • Thompson BJ, Cohen SM (2006) The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 126:767–774

    Article  PubMed  CAS  Google Scholar 

  • Truscott M, Islam AB, Lopez-Bigas N et al (2011) mir-11 limits the proapoptotic function of its host gene, dE2f1. Genes Dev 25:1820–1834

    Article  PubMed  CAS  Google Scholar 

  • Tsurudome K, Tsang K, Liao EH et al (2010) The Drosophila miR-310 cluster negatively regulates synaptic strength at the neuromuscular junction. Neuron 68:879–893

    Article  PubMed  CAS  Google Scholar 

  • Tyler DM, Okamura K, Chung WJ et al (2008) Functionally distinct regulatory RNAs generated by bidirectional transcription and processing of microRNA loci. Genes Dev 22:26–36

    Article  PubMed  CAS  Google Scholar 

  • Varghese J, Cohen SM (2007) MicroRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes Dev 21:2277–2282

    Article  PubMed  CAS  Google Scholar 

  • Varghese J, Lim SF, Cohen SM (2010) Drosophila miR-14 regulates insulin production and metabolism through its target, sugarbabe. Genes Dev 24:2748–2753

    Article  PubMed  CAS  Google Scholar 

  • Vasudevan S, Tong Y, Steitz JA (2007) Switching from repression to activation: microRNAs can up-regulate translation. Science 318:1931–1934

    Article  PubMed  CAS  Google Scholar 

  • Viswanathan SR, Daley GQ (2010) Lin28: a microRNA regulator with a macro role. Cell 140:445–449

    Article  PubMed  CAS  Google Scholar 

  • Yue D, Liu H, Huang Y (2009) Survey of computational algorithms for MicroRNA target prediction. Curr Genomics 10:478–492

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Geetanjali Chawla or Nicholas S. Sokol .

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Chawla, G., Sokol, N.S. (2012). MicroRNA Pathways in Drosophila . In: Erdmann, V., Barciszewski, J. (eds) From Nucleic Acids Sequences to Molecular Medicine. RNA Technologies. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27426-8_25

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