Insect MicroRNAs: Biogenesis, expression profiling and biological functions

Insect Biochemistry and Molecular Biology

Volumn 43, Issue 1, 2013, Pages 24-38

  Lucas, Keira ^a   Raikhel, Alexander S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Drosophila; Insect; MicroRNA; MicroRNA biogenesis; MicroRNA function; MicroRNA target; Mosquito; Small non coding RNA

Indexed keywords

MICRORNA;

ANIMAL; BIOSYNTHESIS; GENE EXPRESSION PROFILING; INSECT; METABOLISM; RNA INTERFERENCE; SHORT SURVEY;

ANIMALS; GENE EXPRESSION PROFILING; INSECTS; MICRORNAS; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; DROSOPHILIDAE; FUNGI; HEXAPODA; INVERTEBRATA; VERTEBRATA;

EID: 84870380694     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2012.10.009     Document Type: Short Survey

References (170)

1. Baek D., Villén J., Shin C., Camargo F.D., Gygi S.P., Bartel D.P. The impact of microRNAs on protein output. Nature 2008, 455:64-71.
2. Bazzini A.A., Lee M.T., Giraldez A.J. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in Zebrafish. Science 2012, 336:233-237.
3. Behm-Ansmant I., Rehwinkel J., Izaurralde E. MicroRNAs silence gene expression by repressing protein expression and/or promoting mRNA decay. Cold Spring Harb Symp. Quant Biol. 2006, 71:523-530.
4. Bellés X. Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annu. Rev. Entomol. 2010, 55:111-128.
5. Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409:363-366.
6. Betel D., Wilson M., Gabow A., Marks D.S., Sander C. The resource: targets and expression. Nucl. Acids Res. 2008, 36:D149-D153. http://microRNA.org.
7. Biryukova I., Asmar J., Abdesselem H., Heitzler P. Drosophila mir-9a regulates wing development via fine-tuning expression of the LIM only factor, dLMO. Dev. Biol. 2009, 327:487-496.
8. 2-sensitive receptors in tsetse flies (Diptera: Glossina palpalis). Physiol. Entomol. 1992, 17:19-24.
9. Bohnsack M.T., Czaplinski K., Gorlich D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 2004, 10:185-191.
10. Borchert G.M., Lanier W., Davidson B.L. RNA polymerase III transcribes human miRNAs. Nat. Struct. Mol. Biol. 2006, 13:1097-1101.
11. Boyle M., Wong C., Rocha M., Jones D.L. Decline in self-renewal factors contributes to aging of the stem cell niche in the Drosophila testis. Cell Stem Cell 2007, 1:470-478.
12. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
13. Britton R.J., Davidson E.H. Gene regulation for higher cells: a theory. Science 1969, 165:349-357.
14. Brown S., Holtzman S., Kaufman T., Denell R. Characterization of the Tribolium Deformed ortholog and its ability to directly regulate Deformed target genes in the rescue of a Drosophila Deformed null mutant. Dev. Genes Evol. 1999, 209:389-398.
15. Bryant B., Macdonald W., Raikhel A.S. MicroRNA miR-275 is indispensable for blood digestion and egg development in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. 2010, 107:22391-22398.
16. Cao J., Tong C., Wu X., Lv J., Yang Z., Jin Y. Identification of conserved microRNAs in Bombyx mori (silkworm) and regulation of fibroin L chain production by microRNAs in heterologous system. Insect Biochem. Mol. Bio. 2008, 38:1066-1071.
17. 2 sensory systems. Science 2008, 319:1256-1260.
18. Cenik E.S., Fukunaga R., Lu G., Dutcher R., Wang Y., Tanaka-Hall T.M., Zamore P.D. Phosphate and R2D2 restrict the substrate specificity of Dicer-2, an ATP-driver ribonuclease. Mol. Cell. 2011, 42:172-184.
19. Cheloufi S., Dos Santos C.O., Chong M.M., Hannon G.J. A Dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010, 465:584-589.
20. Chen X., Yu X., Cai Y., Zheng H., Yu D., Liu G., Zhou Q., Hu S., Hu F. Next-generation small RNA sequencing for microRNAs profiling in honey bee Apis mellifera. Insect Mol. Biol. 2010, 19:799-805.
21. Chen Q., Lu L., Hua H., Zhou F., Lu L., Lin Y. Characterisation and comparative analysis of small RNAs in three small RNA libraries of the Brown Planthopper (Nilaparvata lugens). PLoS One 2012, 7:e32860.
22. Chendrimada T.P., Finn K.J., Ji X., Baillat D., Gregory R.I., Liebhaber S.A., Pasquinelli A.E., Shiekhatter R. MicroRNA silencing through RISC recruitment of eIF6. Nature 2007, 447:823-828.
23. Chi S.W., Zang J.B., Mele A., Darnell R.B. Argonaute HITS-CLIP decode microRNA-mRNA interaction maps. Nature 2009, 460:479-486.
24. Choi I.K., Hyun S. Conserved microRNA miR-8 in fat body regulates innate immune homeostasis in Drosophila. Dev. Comp. Immunol. 2012, 37:50-54.
25. Cook H.A., Koppetsch B.S., Wu J., Theurkauf W.E. The Drosophila SDE3 homolog armitage is required for oskar mRNA silencing and embryonic axis specification. Cell 2004, 116:817-829.
26. Cristino A.S., Tanaka E.D., Rubio M., Piulachs M.D., Belles X. Deep sequencing of organ- and stage-specific microRNAs in the evolutionarily basal insect Blattella germanica (L.) (Dictyoptera, Blattellidae). PLoS One 2011, 6:e19350.
27. Denli A.M., Tops B.B., Plasterk R.H., Ketting R.F., Hannon G.J. Processing of primary microRNAs by the Microprocessor complex. Nature 2004, 432:231-235.
28. Djuranovic S., Nahvi A., Green R. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 2012, 336:237-240.
29. Duursma A.M., Kedde M., Schrier M., Le Sage C., Agami R. miR-178 targets human DNMT3b protein coding region. RNA 2008, 14:872-878.
30. Ebert M.S., Neilson J.R., Sharp P.A. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 2007, 4:721-726.
31. Enright A.J., John B., Gaul U., Tuschl T., Sander C., Marks D.S. MicroRNA targets in Drosophila. Genome Biol. 2003, 5:R1.
32. Fire A., Albertson D., Harrison S.W., Moerman D.G. Production of antisense RNA leads to effective and specific inhibition of gene expression in C.elegans muscle. Development 1991, 113:503-514.
33. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
34. Flynt A.S., Greimann J.C., Chung W.J., Lima C.D., Lai E.C. MicroRNA biogenesis via splicing and exosome-mediated trimming in Drosophila. Mol. Cell. 2010, 38:900-907.
35. Forman J.J., Legesse-Miller A., Coller H.A. A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc. Natl. Acad. Sci. USA 2008, 30:14879-14884.
36. Förstemann K., Horwich M.D., Wee L.M., Tomari Y., Zamore P.D. Drosophila microRNAs are sorted into functionally distinct Argonaute protein complexes after their production by Dicer-1. Cell 2007, 130:287-297.
37. Gagan J., Det B.K., Layer R., Yan Z., Dutta A. MicroRNA-378 targets the mycogenic repressor MyoR during myoblast differentiation. J. Biol. Chem. 2011, 286:19431-19438.
38. Ge W., Chen Y.W., Weng R., Lim S.F., Buescher M., Zhang R., Cohen S.M. Overlapping functions of microRNAs in control of apoptosis during Drosophila embryogenesis. Cell. Death Differ. 2012, 19:839-846.
39. Grant A.J., O'Connell R.J. Electrophysiological responses from receptor neurons in mosquito maxillary palp sensilla. Ciba Found. Symp. 1996, 200:233-248.
40. Greenberg J.K., Xia J., Zhou X., Thatcher S.R., Gu X., Ament S.A., Newman T.C., Green P.J., Zhang W., Robinson G.E., Ben-Shahar Y. Behavioral plasticity in honey bees is associated with differences in brain microRNA transcriptome. Genes, Brain Behav. 2012, 10.1111/j.1601-183X.2012.00782.x.
41. Gregory R.I., Yan K.P., Amuthan G., Chendrimada T., Doratotaj B., Cooch N., Shiekhattar R. The Microprocessor complex mediates the genesis of microRNAs. Nature 2004, 432:235-240.
42. Griffiths-Jones D., Grocock R.J., van Dongen S., Bateman A., Enright A.J. miRBase: microRNA sequences, targets and gene nomenclature. Nucl. Acids Res. 2006, 24:D140-D144.
43. Griffiths-Jones S., Saini H.K., van Dongen S., Enright A.J. miRBase: tools for microRNA genomics. Nucl. Acids Res. 2008, 36:D154-D158.
44. Grün D., Wang Y.L., Langenberger D., Gunsalus K.C., Rajewsky N. MicroRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput. Biol. 2005, 1:51-66.
45. Guo S., Kemphues K.J. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 1995, 81:611-620.
46. Guo H., Ingolia N.T., Weissman J.S., Bratel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
47. Hafner M., Landthaler M., Burger L., Khorshid M., Hausser J., Berninger P., Rothballer A., Ascano M., Jungkamp A.C., Munschauer M., Ulrich A., Wardle G.S., Dewell S., Zavolan M., Tuschl T. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010, 141:129-141.
48. Haraguchi T., Ozaki Y., Iba H. Vectors expressing efficient RNA decoys achieve the long-term suppression of specific microRNA activity in mammalian cells. Nucl. Acids Res. 2009, 37:e43.
49. Haraguchi T., Nakano H., Tagawa T., Ohki T., Ueno Y., Yoshida T., Iba H. A potent 2'-O-methylated RNA-based microRNA inhibitor with unique secondary structures. Nucl. Acids Res. 2012, 40:e58.
50. Hamilton A.J., Baulcombe D.C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 1999, 286:950-952.
51. Hammond S.M., Boettcher S., Caudy A.A., Kobayashi R., Hannon G.J. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 2001, 293:1146-1150.
52. Han J., Lee Y., Yeom K.H., Kim Y.K., Jin H., Kim V.N. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 2004, 18:3016-3027.
53. Han J., Lee Y., Yeom K.H., Nam J.W., Heo I., Rhee J.K., Sohn S.Y., Cho Y., Zhang B.T., Kim V.N. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 2006, 125:887-901.
54. Han B.W., Hung J.H., Weng Z., Zamore P.D., Ameres S.L. The 3'-to-5' exoribonuclease Nibber shapes the 3' ends of microRNAs bound to Drosophila Argonaute1. Curr. Biol. 2011, 21:1878-1887.
55. 2 receptor neuron formation. J. Neurosci. 2011, 31:15660-15673.
56. Hikichi M., Kidokoro M., Haraguchi T., Iba H., Shida H., Tahara H., Nakamura T. MicroRNA regulation of glycoprotein B5R in oncolytic vaccinia virus reduces viral pathogenicity without impairing its antitumor efficacy. Mol. Ther. 2011, 19:1107-1115.
57. Hilgers V., Bushati N., Cohen S.M. Drosophila microRNAs 263a/b confer robustness during development by protecting nascent sense organs from apoptosis. PLoS Biol. 2010, 8:e1000396.
58. Hofacker I.L., Fontana W., Stadler P.F., Bonhoeffer L.S., Tacker M., Schuster P. Fast folding and comparison of RNA secondary structures. Monatshefte Chem. 1996, 125:167-188.
59. Horwich M.D., Zamore P.D. Design and delivery of antisense oligonucleotides to block microRNA function in cultured Drosophila and human cells. Nat. Protoc. 2008, 3:1537-1549.
60. Huang Y., Zou Q., Shen X.J., Tang S.M., Wang S.P., Zhao Q.L. Differential expression of microRNA-2b with potential target coding P25 in the fifth instar larvae posterior silk gland of the silkworm. Mol. Biol. (Mosk) 2011, 45:627-632.
61. Hughes C.L., Kaufman T.C. RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the hemipteran head. Development 2000, 127:3683-3694.
62. Hussain M., Asgari S. Functional analysis of a cellular microRNA in insect host-ascovirus interaction. J. Virol. 2010, 84:612-620.
63. Hussain M., Frentiu F.D., Moreira L.A., O'Neil S.L., Asgari S. Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proc. Natl. Acad. Sci. 2011, 108:9250-9255.
64. Hutvánger G., McLachlan J., Paquinelli A.E., Bálint E., Tuschl T., Zamore P.D. A cellular function for the RNA-interference enzyme dicer in the maturation of the let-7 small temporal RNA. Science 2001, 293:834-839.
65. Hyun S., Lee J.H., Jin H., Nam J.W., Namkoong B., Lee G., Chung J., Kim V.N. Conserved MicroRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 2009, 139:1096-1108.
66. Imamura M., Nakai J., Inoue S., Quan G.X., Kanda T., Tamura T. Targeted gene expression using the GAL4/UAS system in the silkworm Bombyx mori. Genetics 2003, 165:1329-1340.
67. Iovino N., Pane A., Gaul U. miR-184 has multiple roles in Drosophila female germline development. Dev. Cell. 2009, 17:123-133.
68. Jagadeeswaran G., Zheng Y., Sumathipala N., Jiang H., Arrese E.L., Soulages J.L., Zhang W., Sunker R. Deep sequencing of small RNA libraries reveals dynamic regulation of conserved and novel microRNAs and microRNA-stars during silkworm development. BMC Genomics 2010, 11:52.
69. Jiang F., Ye X., Liu X., Fincher L., McKearin D., Liu Q. Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes Dev. 2005, 19:1674-1679.
70. Jones W.D., Cayirlioglu P., Kadow I.G., Vosshall L.B. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 2007, 445:86-90.
71. Karres J.S., Hilgers V., Carrera I., Treisman J., Cohen S.M. The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell 2007, 131:136-145.
72. Kellogg F.E. Water vapour and carbon dioxide receptors in Aedes aegypti. J. Insect Physiol. 1970, 16:99-108.
73. Kennell J.A., Gerin I., MacDougald O.A., Cadigan K.M. The microRNA miR-8 is a conserved negative regulator of Wnt signaling. Proc. Natl. Acad. Sci. 2008, 105:15417-15422.
74. Kennell J.A., Cadigan K.M., Shakhmantsir I., Waldron E.J. The microRNA miR-8 is a positive regulator of pigmentation and eclosion in Drosophila. Dev. Dyn. 2012, 241:161-168.
75. Kennerdell J.R., Carthew R.W. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 1998, 95:1017-1026.
76. Kertesz M., Iovino N., Unnerstall U., Gaul U., Segal E. The role of site accessibility in the microRNA target recognition. Nat. Genet. 2007, 39:1278-1284.
77. Ketting R.F., Fischer S.E., Bernstein E., Sijen T., Hannon G.J., Plasterk H.A. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C.elegans. Genes Dev. 2001, 15:2654-2659.
78. Kheradpour P., Stark A., Roy S., Kellis M. Reliable predication of regulator targets using 12 Drosophila genomes. Genome Res. 2007, 17:1919-1931.
79. Kiriakidou M., Tan G.S., Lamprinaki S., De Planell-Saguer M., Nelson P.T., Mourelatos Z. An mRNA m7G cap binding-like motif within human Ago2 represses translation. Cell 2007, 129:1141-1151.
80. Knight S.W., Bass B.L. A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science 2001, 293:2269-2271.
81. Kokoza V.A., Raikhel A.S. Targeted gene expression in the transgenic Aedes aegypti using the binary Gal4-UAS system. Insect Biochem. Mol. Biol. 2011, 41:637-644.
82. Krek A., Grün D., Poy M.N., Wolf R., Rosenberg L., Epstein E.J., MacMenamin P., da Piedada I., Gunsalus K.C., Stoffel M., Rajewsky N. Combinatorial microRNA target predictions. Nat. Genet. 2005, 37:495-500.
83. Krüger J., Rehmsmeier RNAhybrid: microRNA target prediction easy, fast and flexible. Nucl. Acids Res. 2006, 34:W451-W454.
84. Krützfeldt J., Rajewsky N., Braich R., Rajeev K.G., Tuschl T., Manoharan M., Stoffel M. Silencing of miRNAs in vivo with " antagomirs" Nature 2005, 238:685-689.
85. Kumarswamy R., Chandna S. Inhibition of microRNA-14 contributes to actinomycin-D-induced apoptosis in the Sf9 insect cell line. Cell. Biol. Int. 2010, 34:851-857.
86. Kwon C., Han Z., Olson E.N., Srivastava D. MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. Proc. Natl. Acad. Sci. 2005, 102:18986-18991.
87. 2 reception in Drosophila. Proc. Natl. Acad. Sci. 2007, 104:3574-3578.
88. Lagos-Quintana M., Rauhut R., Lendeckel W., Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001, 294:853-858.
89. Lall S., Grün D., Krek A., Chen K., Wang Y.L., Dewey C.N., Sood P., Colombo T., Bray N., MacMenamin P., Kao H.L., Gunsalus K.C., Pachter L., Piano F., Rajewsky N. A genome-wide map of conserved microRNA targets in C.elegans. Curr. Biol. 2006, 16:460-471.
90. Landthaler M., Yalcin A., Tuschl T. The human DiGeorge syndrome critical region gene 8 and its D. melanogaster homolog are required for miRNA biogenesis. Curr. Biol. 2004, 14:2162-2167.
91. Lau N.C., Lim L.P., Weinstein E.G., Bartel D.P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001, 294:858-862.
92. Leaman D., Chen P.Y., Fak J., Yalcin A., Pearce M., Unnerstall U., Marks D.S., Sander C., Tuschl T., Gaul U. Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development. Cell 2005, 121:1097-1108.
93. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
94. Lee R.C., Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001, 294:862-864.
95. Lee Y., Jeon K., Lee J.T., Kim S., Kim V.N. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 2002, 21:4663-4670.
96. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., Lee J., Provost P., Radmark O., Kim S., Kim V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425:415-419.
97. Lee Y., Kim M., Han J., Yeom K.H., Lee S., Baek S.H., Kim V.N. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 2004, 23:4051-4060.
98. Lee Y.S., Nakahara K., Pham J.W., Kim K., He Z., Sontheimer E.J., Carthew R.W. Distinct roles for Drosophila dicer-1 and dicer-2 in the siRNA/miRNA silencing pathways. Cell 2004, 117:69-81.
99. Legeai F., Rizk G., Walsh T., Edwards O., Gordon K., Lavenier D., Leterme N., Meréau A., Nicolas J., Tagu D., Jaubert-Possamai S. Bioinformatic prediction, deep sequencing or microRNAs and expression analysis during phenotypic plasticity in the pea aphid, Acyrthosiphon pisum. BMC Genomics 2010, 11:281.
100. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
101. Lewis M.A., Quint E., Glazier A.M., Fuchs H., De Angelis M.H., Langford C., van Dongen S., Abreu-Goodger C., Piipari M., Redshaw N., Dalmay T., Moreno-Pelayo M.A., Enright A.J., Steel K.P. An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat. Genet. 2009, 41:614-618.
102. Li X., Carthew R.W. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 2005, 123:1267-1277.
103. Li X., Cassidy J.J., Reinke C.A., Fischboeck S., Carthew R.W. A microRNA imparts robustness against environmental fluctuation during development. Cell 2009, 137:273-283.
104. Li S., Mead E.A., Liang S., Tu Z. Direct sequencing and expression analysis of a large number of miRNAs in Aedes aegypti and a multi-species survey of novel mosquito miRNAs. BMC Genomics 2009, 10:581.
105. Li Y., Padgett R.W. Bantam is required for optic lobe development and glial cell proliferation. PLoS One 2012, 7:e32910.
106. Liu S., Li D., Li Q., Zhao P., Xiang Z., Xia Q. MicroRNAs of Bombyx mori identified by Solexa sequencing. BMC Genomics 2010, 11:148.
107. Liu N., Abe M., Sabin L.R., Hendriks G.J., Nagvi A.S., Yu Z., Cherry S., Bonini N.M. The exoribonuclease Nibbler controls 3' end processing of microRNAs in Drosophila. Curr.Biol. 2011, 21:1888-1893.
108. Liu N., Landreh M., Cao K., Abe M., Hendriks G.J., Kennerdell J.R., Zhu Y., Wang L.S., Bonini N.M. The microRNA miR-34 modulates ageing and neurodegeneration on Drosphila. Nature 2012, 482:519-523.
109. Liu F., Peng W., Li Z., Li W., Li L., Pan J., Zhang S., Miao Y., Chen S., Su S. Next-generation small RNA sequencing for microRNAs profiling in Apis mellifera: comparison between nurses and foragers. Insect Mol. Biol. 2012, 21:297-303.
110. Loya C.M., Lu C.S., Van Vactor D., Fulga T.A. Transgenic microRNA inhibition with spatiotemporal specificity in intact organisms. Nat. Methods 2009, 6:897-903.
111. Lu Z., Li Y., Takwi A., Li B., Zhang J., Conklin D.J., Young K.H., Martin R., Li Y. miR-301a as an NK-kB activator in pancreatic cancer cells. EMBO J. 2011, 31:57-67.
112. Lund E., Güttinger S., Calado A., Dahlber J.E., Kutay U. Nuclear export of microRNA precursors. Science 2004, 303:95-98.
113. Lynd A., Lycett G.J. Development of the Bi-Partite Gal4-UAS system in the African malaria mosquito, Anopheles gambiae. PLoS One 2012, 7:e31552.
114. Lytle J.R., Yario T.A., Steitz J.A. Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR. Proc. Natl. Acad. Sci. 2007, 104:9667-9672.
115. Maragkakis M., Alexiou P., Papadopoulos G.L., Reczko M., Dalamagas T., Giannopoulos G., Goumas G., Koukis E., Kourtis K., Simossis V.A., Sethupathy P., Vergoulis T., Koziris N., Sellis T., Tsanakas P., Hatzigeorgiou A.G. Accurate microRNA target prediction correlates with protein repression levels. BMC Bioinform. 2009, 10:295.
116. Maragkakis M., Reczko M., Simossis V.A., Alexiou P., Papadopoulos G.L., Dalamagas T., Giannopoulos G., Goumas G., Koukis E., Kourtis K., Vergoulis T., Koziris N., Sellis T., Tsanakas P., Hatzigeorgiou A.G. DIANA-microT web server: elucidating microRNA functions through target prediction. Nucl. Acids Res. 2009, 37:W273-W276.
117. Mead E.A., Tu Z. Cloning, characterization and expression of microRNAs from the Asian malaria mosquito, Anopheles stephensi. BMC Genomics 2008, 9:244.
118. Mencia A., Modamino-Høybiør S., Redshaw N., Morin M., Mayo-Merino F., Olavarrieta L., Aguirre L.A., del Castillo I., Steel K.P., Dalmay T., Moreno F., Moreno-Pelayo M.A. Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat. Genet. 2009, 41:609-613.
119. Moretti F., Kaiser C., Zdanowicz-Specht A., Hentze M.W. PABP and the poly(A) tail augment microRNA repression by facilitated miRISC binding. Nat. Str. Mol. Biol. 2012, 19:603-608.
120. Napoli C., Lemieux C., Jorgensen R. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. The Plant Cell 1990, 2:279-289.
121. Okamura K., Ishizuka A., Siomi H., Siomi M.C. Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 2004, 18:1655-1666.
122. Okamura K., Hagen J.W., Duan H., Tyler D.M., Lai E.C. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 2007, 130:89-100.
123. Okamura K., Liu N., Lai E.C. Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. Mol. Cell. 2009, 36:431-444.
124. Orom U.A., Nielsen F.C., Lund A.H. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell. 2008, 30:460-471.
125. Pek J.W., Lim A.K., Kai T. Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev. Cell. 2009, 17:417-424.
126. Petersen C.P., Bordeleau M.E., Pelletier J., Sharp P.A. Short RNAs repress translation after initiation in mammalian cells. Mol. Cell. 2006, 21:533-542.
127. Rehmsmeier M., Steffen P., Hochsmann M., Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA 2004, 10:1507-1517.
128. Rehwinkel J., Behm-Ansmant I., Gatfield D., Izaurralde E. A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 2005, 11:1640-1647.
129. Reinhart B.J., Slack F.J., Basson M., Pasquinelli A.E., Bettinger J.C., Rougvie A.E., Horvitz H.R., Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 409:901-906.
130. Rodriguez A., Griffiths-Jones S., Ashurst J.L., Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res. 2004, 14:1902-1910.
131. Ronshaugen M., Biemar F., Piel J., Levine M., Lai E.C. The Drosophila microRNA iab-4 causes a dominant homeotic transformation of halteres to wings. Genes Dev. 2005, 19:2947-2952.
132. Rusinov V., Baev V., Minkov I.N., Tabler M. MicroInspector: a web tool for detection of miRNA binding sites in an RNA sequence. Nucl. Acid Res. 2005, 33:W696-W700.
133. Ruby J.G., Stark A., Johnston W.K., Kellis M., Bartel D.P., Lai E.C. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res. 2007, 14:1850-1864.
134. Ruby J.G., Jan C.H., Bartel D.P. Intronic microRNA precursors that bypass Drosha processing. Nature 2007, 448:83-86.
135. Saito K., Ishizuka A., Siomi H., Siomi M.C. Processing of pre-microRNAs by the dicer-1-loquacious complex in Drosophila cells. PLoS Biol. 2005, 3:1202-1212.
136. Schinko J.B., Weber M., Viktorinova I., Kiupakis A., Averof M., Klinger M., Wimmer E.A., Bucher G. Functionality of the GAL4/UAS system in Tribolium requires the use of endogenous core promoters. BMC Dev. Bio. 2010, 10:53.
137. Selbach M., Schwanhäusser B., Thierfelder N., Fang Z., Khanin R., Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455:58-63.
138. Shen W.F., Hu Y.L., Uttarwar L., Passeque E., Largman C. MicroRNA-126 regulates HOXA9 by binding to the homeobox. Mol. Cel Biol. 2008, 28:4609-4619.
139. Silver S.J., Hagen J.W., Okamura K., Perrimin N., Lai E.C. Functional screening identifies miR-315as a potent activator of Wingless signaling. Proc. Natl. Acad. Sci. 2007, 104:18151-18156.
140. Skalsky R.L., Vanlandingham D.L., Scholle F., Higgs S., Cullen B.R. Identification of microRNAs expressed in two mosquito vectors, Aedes albopictus and Culex quinquefasciatus. BMC Genomics 2010, 11:119.
141. Sokol N.S., Xu P., Jan Y.N., Ambros V. Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes Dev. 2008, 22:1591-1596.
142. Stenvang J., Perti A., Lindow M., Obad S., Kauppinen S. Inhibition of microRNA function by antimiR oligonucleotides. Silence 2012, 3. 10.1186/1758-907X-3-1.
143. Surridge A.K., Lopez-Gomollon S., Moxon S., Maroja L.S., Rathjen T., Nadeau N.J., Dalmay T., Jiggens C.D. Characterisation and expression of microRNAs in developing wings of the neotropical butterfly Heliconius melpomene. BMC Genomics 2011, 12:62.
144. Tan H., Poidevin M., Li H., Chen D., Jin P. MicroRNA-277 modulates the neurodegeneration caused by Fragile X permutation rCGG repeats. PLoS Genet. 2012, 8:e1002681.
145. Tay Y., Zhang J., Thomson A.M., Lim B., Rigoutsos I. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008, 455:1124-1128.
146. Teleman A.A., Maitra S., Cohen S.M. Drosophila lacking microRNA miR-278 are defective in energy homeostasis. Genes Dev. 2006, 20:417-422.
147. Toledano H., D'Alterio C., Czech B., Levine E., Jones D.L. The let-7-imp axis regulates aging of the Drosophila testis stem-cell niche. Nature 2012, 485:605-610.
148. Tomari Y., Du T., Zamore P.D. Sorting of Drosophila small silencing RNAs. Cell 2007, 130:299-308.
149. Truscott M., Islam A.B., López-Bigas N., Frolov M.V. mir-11 limits the proapoptotic function of its host gene, dE2f1. Genes Dev. 2012, 25:1820-1834.
150. Tsurudome K., Tsang K., Liao E.H., Ball R., Penney J., Yang J.S., Elazzauzi F., He T., Chishti A., Lnenicka G., Lai E.C., Haghighi A.P. The Drosophila miR-310 cluster negatively regulates synaptic strength at the neuromuscular junction. Neuron 2010, 68:879-893.
151. Tsutsumi A., Kawamata T., Izumi N., Seitz H., Tomari Y. Recognition of the pre-miRNA structure by Drosophila Dicer-1. Nat. Struct. Mol. Biol. 2011, 18:1153-1158.
152. Vallejo D.M., Caparros E., Dominguez M. Targeting Notch signaling by the conserved miR8/200 microRNA family in development and cancer cells. EMBO J. 2011, 30:756-759.
153. van der Krol A.R., Mur L.A., Beld M., Mol J.N., Stuitje A.R. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. The Plant Cell 1990, 2:291-299.
154. Varghese J., Cohen S.M. MicroRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes Dev. 2007, 21:2277-2282.
155. Varghese J., Lim S.F., Cohen Drosophila miR-14 regulates insulin production and metabolism through its target, sugarbabe. Genes Dev. 2010, 24:2748-2753.
156. Wang X. miRDB: a microRNA target prediction and functional annotation database with a wiki interface. RNA 2008, 14:1012-1017.
157. Wang X., El Naqa I.M. Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics 2008, 24:325-332.
158. Weng R., Cohen S.M. Drosophila miR-124 regulates neuroblast proliferation through its target anachronism. Development 2012, 139:1427-1434.
159. Wightman B., Ha I., Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75:855-862.
160. Winter F., Edaye S., Hüttenhofer A., Brunel C. Anopheles gambiae miRNAs as actors of defence reaction against Plasmodium invasion. Nucl. Acids Res. 2007, 35:6953-6962.
161. Xiao F., Zuo Z., Cai G., Kang S., Gao X., Li T. miRecords: an integrated resource for microRNA-target interactions. Nucl. Acids Res. 2009, 37:D105-D110.
162. Xu P., Vernooy S.Y., Gou M., Hay B.A. The Drosophila microRNA Mir-14 suppresses cell death and is required for normal fat metabolism. Curr. Biol. 2003, 13:790-795.
163. Yang Y., Chaerkady R., Kandasamy K., Huang T.C., Selvan L.D., Dwivedi S.B., Kent O.A., Mendell J.T., Pandey A. Identifying targets of miR-143 using a SILAC-based proteomic approach. Mol. Biosyst. 2010, 6:1873-1882.
164. Yang L., Lu X., Liu Y., Chen J., Yu W., Zhang Y., Nie Z. Expression analysis of miRNAs in BmN cells. Gene 2012, 505:240-450.
165. Yi R., Qin Y., Macara I.G., Cullen B.R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003, 17:3011-3016.
166. Yu X., Zhou Q., Li S.C., Lou Q., Cai Y., Lin W.C., Chen H., Yang Y., Hu S., Yu J. The silkworm (Bombyx mori) microRNAs and their expressions in multiple developmental stages. PLoS One 2008, 3:e2997.
167. Yu J.Y., Reynolds S.H., Hatfield S.D., Shcherbata H.R., Fischer K.A., Ward E.J., Long D., Ding Y., Ruohola-Baker H. Dicer-1-dependent Decapo suppression acts downstream of Insulin receptor in regulating cell division of Drosophila germline stem cells. Development 2009, 136:1497-1507.
168. Zhang Y., Zhou X., Ge X., Jiang J., Li M., Jia S., Yang X., Kan Y., Miao X., Zhao G., Li F., Huang Y. Insect-specific microRNA involved in the development of the silkworm Bombyx mori. PLoS One 2009, 4:e4677.
169. Zhang X., Zheng Y., Jagadeeswaran G., Ren R., Sunkar R., Jiang H. Identification and developmental profiling of conserved and nocel microRNAs in Manduca sexta. Insect Biochem. Mol. Biol. 2012, 42:381-395.
170. Zovoilis A., Agbermenyah H.Y., Agis-Balboa R.C., Stilling R.M., Edbauer D., Rao P., Farinelli L., Delalle I., Schmitt A., Falkai P., Bahari-Javan A., Bukhardt S., Sananbenesi F., Fischer A. MicroRNA-34c is a novel target to treat dementias. EMBO J. 2011, 30:4299-4308.