The impact of age, biogenesis, and genomic clustering on Drosophila microRNA evolution

RNA

Volumn 19, Issue 9, 2013, Pages 1295-1308

  Mohammed, Jaaved ^a,b   Flynt, Alex S ^c   Siepel, Adam ^a   Lai, Eric C ^c  

^a Program on Infrastructure Policy   (United States)

^b Tri Institutional Training Program in Computational Biology and Medicine   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Drosophila; MicroRNA clusters; MicroRNA evolution; Mirtrons; Structure evolution

Indexed keywords

GENOMIC RNA; MICRORNA; SHORT HAIRPIN RNA; UNTRANSLATED RNA;

AGE; ARTICLE; BIOGENESIS; CLUSTER ANALYSIS; DROSOPHILA MELANOGASTER; DYNAMICS; GENE ACTIVITY; GENETIC CONSERVATION; GENOME ANALYSIS; GENOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; RNA STRUCTURE; SEQUENCE ALIGNMENT;

DROSOPHILA; MICRORNA CLUSTERS; MICRORNA EVOLUTION; MIRTRONS; STRUCTURE EVOLUTION;

ANIMALS; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; DROSOPHILA; EVOLUTION, MOLECULAR; GENOME, INSECT; MICRORNAS; MODELS, GENETIC; MULTIGENE FAMILY;

EID: 84883192958     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.039248.113     Document Type: Article

References (50)

1. Altuvia Y, Landgraf P, Lithwick G, Elefant N, Pfeffer S, Aravin A, Brownstein MJ, Tuschl T, Margalit H. 2005. Clustering and conservation patterns of human microRNAs. Nucleic Acids Res 33: 2697-2706.
2. Aravin A, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, Gaasterland T, Meyer J, Tuschl T. 2003. The small RNA profile during Drosophila melanogaster development. Dev Cell 5: 337-350.
3. Auyeung VC, Ulitsky I, McGeary SE, Bartel DP. 2013. Beyond secondary structure: Primary-sequence determinants license Pri-miRNA hairpins for processing. Cell 152: 844-858.
4. Axtell MJ, Westholm JO, Lai EC. 2011. Vive la différence: Biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12: 221.
5. Batzoglou S, Jaffe DB, Stanley K, Butler J, Gnerre S, Mauceli E, Berger B, Mesirov JP, Lander ES. 2002. ARACHNE: A whole-genome shotgun assembler. Genome Res 12: 177-189.
6. 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.
7. Berezikov E, Liu N, Flynt AS, Hodges E, Rooks M, Hannon GJ, Lai EC. 2010. Evolutionary flux of canonical microRNAs and mirtrons in Drosophila. Nat Genet 42: 6-9.
8. Berezikov E, Robine N, Samsonova A, Westholm JO, Naqvi A, Hung JH, Okamura K, Dai Q, Bortolamiol-Becet D, Martin R, et al. 2011. Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence. Genome Res 21: 203-215.
9. Blanchette M, Kent WJ, Riemer C, Elnitski L, Smit AF, Roskin KM, Baertsch R, Rosenbloom K, Clawson H, Green ED, et al. 2004. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res 14: 708-715.
10. Bradley RK, Roberts A, Smoot M, Juvekar S, Do J, Dewey C, Holmes I, Pachter L. 2009. Fast statistical alignment. PLoS Comput Biol 5: e1000392.
11. Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, Baek D, Johnston WK, Russ C, Luo S, Babiarz JE, et al. 2010. Mammalian microRNAs: Experimental evaluation of novel and previously annotated genes. Genes Dev 24: 992-1009.
12. Chung WJ, Agius P, Westholm JO, Chen M, Okamura K, Robine N, Leslie CS, Lai EC. 2011. Computational and experimental identification of mirtrons in Drosophila melanogaster and Caenorhabditis elegans. Genome Res 21: 286-300.
13. Czech B, Hannon GJ. 2010. Small RNA sorting: Matchmaking for Argonautes. Nat Rev Genet 12: 19-31.
14. Drosophila 12 Genomes Consortium, Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, et al. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218.
15. Flynt AS, Lai EC. 2008. Biological principles of microRNA-mediated regulation: Shared themes amid diversity. Nat Rev Genet 9: 831-842.
16. Flynt AS, Chung WJ, Greimann JC, Lima CD, Lai EC. 2010. microRNA biogenesis via splicing and exosome-mediated trimming in Drosophila. Mol Cell 38: 900-907.
17. Friedlander MR, Mackowiak SD, Li N, Chen W, Rajewsky N. 2012. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 40: 37-52.
18. Friedman RC, Farh KK, Burge CB, Bartel DP. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
19. Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK, Sohn SY, Cho Y, Zhang BT, Kim VN. 2006. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125: 887-901.
20. Harris RS. 2007. Improved pairwise alignment of genomic DNA. Center for Comparative Genomics and Bioinformatics. Pennsylvania State University, University Park, PA.
21. Hochsmann M, Toller T, Giegerich R, Kurtz S. 2003. Local similarity in RNA secondary structures. Proc IEEE Comput Soc Bioinform Conf 2: 159-168.
22. Hochsmann M, Voss B, Giegerich R. 2004. Pure multiple RNA secondary structure alignments: A progressive profile approach. IEEE/ACM Trans Comput Biol Bioinform 1: 53-62.
23. Hubisz MJ, Pollard KS, Siepel A. 2011. PHAST and RPHAST: Phylogenetic analysis with space/time models. Brief Bioinform 12: 41-51.
24. Kim YK, Kim VN. 2007. Processing of intronic microRNAs. EMBO J 26: 775-783.
25. Kozomara A, Griffiths-Jones S. 2011. miRBase: Integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39: D152-D157.
26. Ladewig E, Okamura K, Flynt AS, Westholm JO, Lai EC. 2012. Discovery of hundreds of mirtrons in mouse and human small RNA data. Genome Res 22: 1634-1645.
27. Lai EC, Tomancak P, Williams RW, Rubin GM. 2003. Computational identification of Drosophila microRNA genes. Genome Biol 4: R42.41-R42.20.
28. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
29. Lim L, Lau N, Weinstein E, Abdelhakim A, Yekta S, Rhoades M, Burge C, Bartel D. 2003a. The microRNAs of Caenorhabditis elegans. Genes Dev 17: 991-1008.
30. Lim LP, Glasner ME, Yekta S, Burge CB, Bartel DP. 2003b. Vertebrate microRNA genes. Science 299: 1540.
31. Lorenz R, Bernhart SH, Honer Zu Siederdissen C, Tafer H, Flamm C, Stadler PF, Hofacker IL. 2011. ViennaRNA Package 2.0. Algorithms Mol Biol 6: 26.
32. Lu J, Fu Y, Kumar S, Shen Y, Zeng K, Carthew R, Wu CI. 2008a. Adaptive evolution of newly emerged micro-RNA genes in Drosophila. Mol Biol Evol 25: 929-938.
33. Lu J, Shen Y, Wu Q, Kumar S, He B, Shi S, Carthew RW, Wang SM, Wu CI. 2008b. The birth and death of microRNA genes in Drosophila. Nat Genet 40: 351-355.
34. Marygold SJ, Leyland PC, Seal RL, Goodman JL, Thurmond J, Strelets VB, Wilson RJ. 2013. FlyBase: Improvements to the bibliography. Nucleic Acids Res 41: D751-D757.
35. Morlando M, Ballarino M, Gromak N, Pagano F, Bozzoni I, Proudfoot NJ. 2008. Primary microRNA transcripts are processed co-transcriptionally. Nat Struct Mol Biol 15: 902-909.
36. Nobrega MA, Ovcharenko I, Afzal V, Rubin EM. 2003. Scanning human gene deserts for long-range enhancers. Science 302: 413.
37. Nozawa M, Miura S, Nei M. 2010. Origins and evolution of microRNA genes in Drosophila species. Genome Biol Evol 2: 180-189.
38. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC. 2007. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130: 89-100.
39. Okamura K, Phillips MD, Tyler DM, Duan H, Chou YT, Lai EC. 2008. The regulatory activity of microRNA* species has substantial influence on microRNA and 3' UTR evolution. Nat Struct Mol Biol 15: 354-363.
40. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A. 2010. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20: 110-121.
41. Price N, Cartwright RA, Sabath N, Graur D, Azevedo RB. 2011. Neutral evolution of robustness in Drosophila microRNA precursors. Mol Biol Evol 28: 2115-2123.
42. Ruby JG, Jan CH, Bartel DP. 2007a. Intronic microRNA precursors that bypass Drosha processing. Nature 448: 83-86.
43. Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC. 2007b. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 17: 1850-1864.
44. Siepel A, Diekhans M, Brejova B, Langton L, Stevens M, Comstock CL, Davis C, Ewing B, Oommen S, Lau C, et al. 2007. Targeted discovery of novel human exons by comparative genomics. Genome Res 17: 1763-1773.
45. Srivastava A, Cai L, Mrazek J, Malmberg RL. 2011. Mutational patterns in RNA secondary structure evolution examined in three RNA families. PLoS ONE 6: e20484.
46. Stark A, Kheradpour P, Parts L, Brennecke J, Hodges E, Hannon GJ, Kellis M. 2007a. Systematic discovery and characterization of fly microRNAs using 12 Drosophila genomes. GenomeRes 17: 1865-1879.
47. Stark A, Lin MF, Kheradpour P, Pedersen JS, Parts L, Carlson JW, Crosby MA, Rasmussen MD, Roy S, Deoras AN, et al. 2007b. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450: 219-232.
48. Uva P, Da Sacco L, Del Corno M, Baldassarre A, Sestili P, Orsini M, Palma A, Gessani S, Masotti A. 2013. Rat mir-155 generated from the lncRNA Bic is 'hidden' in the alternate genomic assembly and reveals the existence of novel mammalian miRNAs and clusters. RNA 19: 365-379.
49. Yang JS, Lai EC. 2011. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol Cell 43: 892-903.
50. Yang JS, Phillips MD, Betel D, Mu P, Ventura A, Siepel AC, Chen KC, Lai EC. 2011. Widespread regulatory activity of vertebrate microRNA* species. RNA 17: 312-326.