Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs

Genome Research

Volumn 17, Issue 12, 2007, Pages 1850-1864

  Ruby, J Graham ^a,b   Stark, Alexander ^c,d   Johnston, Wendy K ^a,b   Kellis, Manolis ^c,d   Bartel, David P ^a,b   Lai, Eric C ^e  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MESSENGER RNA;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EVOLUTIONARY HOMOLOGY; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; INSECT GENETICS; MATHEMATICAL COMPUTING; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BIOLOGY; BIOSYNTHESIS; COMPARATIVE STUDY; CONFORMATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PRENATAL DEVELOPMENT;

DROSOPHILA MELANOGASTER;

ANIMALS; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICRORNAS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA, MESSENGER;

EID: 38149071979     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.6597907     Document Type: Article

References (65)

1. Abbott, A.L., Alvarez-Saavedra, E., Miska, E.A., Lau, N.C., Bartel, D.P., Horvitz, H.R., and Ambros, V. 2005. The let-7 microRNA family members mir-48, mir-84, and mir-241 function together to regulate developmental timing in Caenorhabditis elegans. Dev. Cell 9: 403-414.
2. Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D., Amanatides, P.G., Scherer, S.E., Li, P.W., Hoskins, R.A., Galle, R.F., et al. 2000. The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
4. Ambros, V., Lee, R.C., Lavanway, A., Williams, P.T., and Jewell, D. 2003. MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr. Biol. 13: 807-818.
5. Aravin, A.A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., Gaasterland, T., Meyer, J., and Tuschl, T. 2003. The small RNA profile during Drosophila melanogaster development. Dev. Cell 5: 337-350.
6. Bartel, D.P. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
7. Baskerville, S. and Bartel, D.P. 2005. Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11: 241-247.
8. Basyuk, E., Suavet, F., Doglio, A., Bordonne, R., and Bertrand, E. 2003. Human let-7 stem-loop precursors harbor features of RNase III cleavage products. Nucleic Acids Res. 31: 6593-6597.
9. Bentwich, I., Avniel, A., Karov, Y., Aharonov, R., Gilad, S., Barad, O., Barzilai, A., Einat, P., Einav, U., Meiri, E., et al. 2005. Identification of hundreds of conserved and nonconserved human microRNAs. Nat. Genet. 37: 766-770.
10. Berezikov, E., Guryev, V., van de Belt, J., Wienholds, E., Plasterk, R.H., and Cuppen, E. 2005. Phylogenetic shadowing and computational identification of human microRNA genes. Cell 120: 21-24.
11. Berezikov, E., Thuemmler, F., van Laake, L.W., Kondova, I., Bontrop, R., Cuppen, E., and Plasterk, R.H. 2006. Diversity of microRNAs in human and chimpanzee brain. Nat. Genet. 38: 1375-1377.
12. Beverley, S.M. and Wilson, A.C. 1984. Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. J. Mol. Evol. 21: 1-13.
13. Brennecke, J., Stark, A., Russell, R.B., and Cohen, S.M. 2005. Principles of microRNA-target recognition. PLoS Biol. 3: e85. doi: 10.1371/journal.pbio.0030085.
14. Crosby, M.A., Goodman, J.L., Strelets, V.B., Zhang, P., and Gelbart, W.M. 2007. FlyBase: Genomes by the dozen. Nucleic Acids Res. 35: D486-D491. doi: 10.1093/nar/gkl827.
15. Cumberledge, S., Zaratzian, A., and Sakonju, S. 1990. Characterization of two RNAs transcribed from the cis-regulatory region of the abd-A domain within the Drosophila bithorax complex. Proc. Natl. Acad. Sci. 87: 3259-3263.
16. Doench, J.G. and Sharp, P.A. 2004. Specificity of microRNA target selection in translational repression. Genes & Dev. 18: 504-511.
17. Drosophila 12 Genomes Consortium. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature (in press) doi: 10.1038/nature06341.
18. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. 95: 14863-14868.
19. Enright, A.J., John, B., Gaul, U., Tuschl, T., Sander, C., and Marks, D.S. 2003. MicroRNA targets in Drosophila. Genome Biol. 5: R1. doi: 10.1186/gb-2003-5-1-r1.
20. Fahlgren, N., Howell, M.D., Kasschau, K.D., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., Givan, S.A., Law, T.F., Grant, S.R., Dangl, J.L., et al. 2007. High-throughput sequencing of Arabidopsis microRNAs: Evidence for frequent birth and death of miRNA genes. PLoS ONE 2: e219. doi: 10.1371/journal.pone.0000219.
21. Farh, K.K., Grimson, A., Jan, C., Lewis, B.P., Johnston, W.K., Lim, L.P., Burge, C.B., and Bartel, D.P. 2005. The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science 310: 1817-1821.
22. Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.L., and Postlethwait, J. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531-1545.
23. Grad, Y., Aach, J., Hayes, G.D., Reinhart, B.J., Church, G.M., Ruvkun, G., and Kim, J. 2003. Computational and experimental identification of C. elegans microRNAs. Mol. Cell 11: 1253-1263.
24. Griffiths-Jones, S. 2004. The microRNA Registry. Nucleic Acids Res. 32: D109-D111. doi: 10.1093/nar/gkh023.
25. Grun, D., Wang, Y.L., Langenberger, D., Gunsalus, K.C., and Rajewsky, N. 2005. microRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput. Biol. 1: e13. doi: 10.1371/journal.pcbi.0010013.
26. Han, J., Lee, Y., Yeom, K.H., Nam, J.W., Heo, I., Rhee, J.K., Sohn, S.Y., Cho, Y., Zhang, B.T., and Kim, V.N. 2006. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125: 887-901.
27. Hofacker, I.L., Fontana, W., Stadler, P.F., Bonhoeffer, L.S., Tacker, M., and Schuster, P. 1994. Fast folding and comparison of RNA secondary structures. Monatsh. Chem. 125: 167-188.
28. Johnston, R.J. and Hobert, O. 2003. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426: 845-849.
29. Karolchik, D., Baertsch, R., Diekhans, M., Furey, T.S., Hinrichs, A., Lu, Y.T., Roskin, K.M., Schwartz, M., Sugnet, C.W., Thomas, D.J., et al. 2003. The UCSC Genome Browser database. Nucleic Acids Res. 31: 51-54.
30. Kheradpour, P., Stark, A., Roy, S., and Kellis, M. 2007. Reliable prediction of regulator targets using 12 Drosophila genomes. Genome Res. (this issue).
31. Khvorova, A., Reynolds, A., and Jayasena, S.D. 2003. Functional siRNAs and miRNAs exhibit strand bias. Cell 115: 209-216.
32. Krek, A., Grun, D., Poy, M.N., Wolf, R., Rosenberg, L., Epstein, E.J., MacMenamin, P., da Piedade, I., Gunsalus, K.C., Stoffel, M., et al. 2005. Combinatorial microRNA target predictions. Nat. Genet. 37: 495-500.
33. Lachaise, D., Cariou, M.L., David, J.R., Lemeunier, F., Tsacas, L., and Ashburner, M. 1988. Historical biogeography of the Drosophila melanogaster species subgroup. Evol. Biol. 22: 159-225.
34. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. 2001. Identification of novel genes coding for small expressed RNAs. Science 294: 853-858.
35. Lai, E.C. 2002. Micro RNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 30: 363-364.
36. Lai, E.C., Tomancak, P., Williams, R.W., and Rubin, G.M. 2003. Computational identification of Drosophila microRNA genes. Genome Biol. 4: R42. doi: 10.1186/gb-2003-4-7-r42.
37. Lai, E.C., Wiel, C., and Rubin, G.M. 2004. Complementary miRNA pairs suggest a regulatory role for miRNA:miRNA duplexes. RNA 10: 171-175.
38. Lai, E.C., Tam, B., and Rubin, G.M. 2005. Pervasive regulation of Drosophila Notch target genes by GY-box-, Brd-box-, and K-box-class microRNAs. Genes & Dev. 19: 1067-1080.
39. Lau, N.C., Lim, L.P., Weinstein, E.G., and Bartel, D.P. 2001. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294: 858-862.
40. Lee, R.C., Feinbaum, R.L., and Ambros, V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854.
41. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S., et al. 2003. The nuclear RNase III Drosha initiates microRNA processing. Nature 425: 415-419.
42. Lewis, B.P., Shih, I.H., Jones-Rhoades, M.W., Bartel, D.P., and Burge, C.B. 2003. Prediction of mammalian microRNA targets. Cell 115: 787-798.
43. Lewis, B.P., Burge, C.B., and Bartel, D.P. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
44. Li, J., Yang, Z., Yu, B., Liu, J., and Chen, X. 2005. Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr. Biol. 15: 1501-1507.
45. Lim, L.P., Glasner, M.E., Yekta, S., Burge, C.B., and Bartel, D.P. 2003a. Vertebrate microRNA genes. Science 299: 1540.
46. Lim, L.P., Lau, N.C., Weinstein, E.G., Abdelhakim, A., Yekta, S., Rhoades, M.W., Burge, C.B., and Bartel, D.P. 2003b. The microRNAs of Caenorhabditis elegans. Genes & Dev. 17: 991-1008.
47. Lim, L.P., Lau, N.C., Garrett-Engele, P., Grimson, A., Schelter, J.M., Castle, J., Bartel, D.P., Linsley, P.S., and Johnson, J.M. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773.
48. Lu, C., Kulkarni, K., Souret, F.F., Muthu Valliappan, R., Tej, S.S., Poethig, R.S., Henderson, I.R., Jacobsen, S.E., Wang, W., Green, P.J., et al. 2006. MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res. 16: 1276-1288.
49. Margulies, M., Egholm, M., Altman, W.E., Attiya, S., Bader, J.S., Bemben, L.A., Berka, J., Braverman, M.S., Chen, Y.J., Chen, Z., et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
50. Ohler, U., Yekta, S., Lim, L.P., Bartel, D.P., and Burge, C.B. 2004. Patterns of flanking sequence conservation and a characteristic upstream motif for microRNA gene identification. RNA 10: 1309-1322.
51. Ohno, S. 1970. Evolution by gene duplication. Springer-Verlag, Berlin, New York.
52. Rajagopalan, R., Vaucheret, H., Trejo, J., and Bartel, D.P. 2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes & Dev. 20: 3407-3425.
53. Richards, S., Liu, Y., Bettencourt, B.R., Hradecky, P., Letovsky, S., Nielsen, R., Thornton, K., Hubisz, M.J., Chen, R., Meisel, R.P., et al. 2005. Comparative genome sequencing of Drosophila pseudoobscura: Chromosomal, gene, and cis-element evolution. Genome Res. 15: 1-18.
54. Riddle, N.C. and Elgin, S.C. 2006. The dot chromosome of Drosophila: Insights into chromatin states and their change over evolutionary time. Chromosome Res. 14: 405-416.
55. Ruby, J.G., Jan, C., Player, C., Axtell, M.J., Lee, W., Nusbaum, C., Ge, H., and Bartel, D.P. 2006. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127: 1193-1207.
56. Ruby, J.G., Jan, C.H., and Bartel, D.P. 2007. Intronic microRNA precursors that bypass Drosha processing. Nature 448: 83-86.
57. Schwartz, A.S. and Pachter, L. 2007. Multiple alignment by sequence annealing. Bioinformatics 23: e24-e29. doi: 10.1093/ bioinformatics/btl311.
58. Schwarz, D.S., Hutvagner, G., Du, T., Xu, Z., Aronin, N., and Zamore, P.D. 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115: 199-208.
59. Sempere, L.F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., and Ambros, V. 2004. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5: R13. http://genomebiology.com/2004/5/3/R13.
60. Stark, A., Brennecke, J., Russell, R.B., and Cohen, S.M. 2003. Identification of Drosophila microRNA targets. PLoS Biol. 1: e60. doi: 10.1371/journal.pbio.0000060.
61. Stark, A., Brennecke, J., Bushati, N., Russell, R.B., and Cohen, S.M. 2005. Animal microRNAs confer robustness to gene expression and have a significant impact on 3′UTR evolution. Cell 123: 1133-1146.
62. Stark, A., Kheradpour, P., Parts, L., Brennecke, J., Hodges, E., Hannon, G.J., and Kellis, M. 2007. Systematic discovery and characterization of fly microRNAs using 12 Drosophila genomes. Genome Res. (this issue). doi: 10.1101/gr.6593807.
63. Stark, A., Lin, M.F., Kheradpour, P., Pedersen, J.S., Parts, L., Carlson, J.W., Crosby, M.A., Rasmussen, M.D., Roy, S., Deoras, A.N., et al. 2007c. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature (in press) doi: 10.1038/nature06340.
64. Wang, H., Ach, R.A., and Curry, B. 2007. Direct and sensitive miRNA profiling from low-input total RNA. RNA 13: 151-159.
65. Wightman, B., Ha, I., and Ruvkun, G. 1993. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75: 855-862.