MicroRNAs in the Same Clusters Evolve to Coordinately Regulate Functionally Related Genes

Molecular Biology and Evolution

Volumn 33, Issue 9, 2016, Pages 2232-2247

  Wang, Yirong ^a,b   Luo, Junjie ^a   Zhang, Hong ^a   Lu, Jian ^a  

^a Tsinghua University   (China)

^b PEKING UNIVERSITY   (China)

Author keywords

coordinated regulation; evolution; functional co adaptation; MIR 17 92 cluster; miRNA clusters; mRNA Seq; natural selection

Indexed keywords

MICRORNA; TRANSCRIPTOME;

ANIMAL CELL; ARTICLE; CHICKEN; CONTROLLED STUDY; DIPTERA; GENE CLUSTER; GENE CONTROL; GENE DUPLICATION; GENE EXPRESSION; HUMAN; INSECT CELL; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; OVERLAPPING GENE; RNA INTERFERENCE; RNA SEQUENCE; RNA TRANSCRIPTION; RNA TRANSPORT; WORM; ZEBRA FISH; ANIMAL; CLUSTER ANALYSIS; CONSERVED SEQUENCE; EVOLUTION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETICS; GENOMICS; HIGH THROUGHPUT SEQUENCING; MULTIGENE FAMILY; PROCEDURES; SEQUENCE ANALYSIS;

ANIMALS; BIOLOGICAL EVOLUTION; CLUSTER ANALYSIS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MICRORNAS; MULTIGENE FAMILY; SELECTION, GENETIC; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84995407029     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw089     Document Type: Article

References (85)

1. Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, Korbel JO, Marchini JL, McCarthy S McVean GA. 1000 Genomes Project Consortium, et al. 2015. A global reference for human genetic variation. Nature 526:68-74.
2. Agarwal V, Bell GW, Nam J-W, Bartel DP. 2015. Predicting effective microRNA target sites in mammalian mRNAs. Elife 4:e05005.
3. 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.
4. Ambros V. 2003. MicroRNA pathways in flies and worms: growth, death, fat, stress, timing. Cell 113:673-676.
5. Bartel DP. 2004. MicroRNAs: genomics, biogenesis, mechanism, function. Cell 116:281-297.
6. Bartel DP. 2009. MicroRNA target recognition and regulatory functions. Cell 136:215-233.
7. Baskerville S, Bartel DP. 2005. Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11:241-247.
8. Bazzini AA, Lee MT, Giraldez AJ. 2012. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336:233-237.
9. Berezikov E, Robine N, Samsonova A, Westholm JO, Naqvi A, Hung J-H, Okamura K, Dai Q, Bortolamiol-Becet D, Martin R, et al. 2011. Deep annotation of Drosophila melanogaster microRNAs yields insights into their processing, modification, emergence. Genome Res. 21:203-215.
10. Berezikov E, van Tetering G, Verheul M, van de Belt J, van Laake L, Vos J, Verloop R, van de Wetering M, Guryev V, Takada S, et al. 2006. Evolutionary flux of canonical microRNAs and mirtrons in Drosophila. Genome Res. 16:6-9. author reply 9-10.
11. Brawand D, Soumillon M, Necsulea A, Julien P, Cs-ardi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, et al. 2011. The evolution of gene expression levels in mammalian organs. Nature 478:343-348.
12. Chen S, Krinsky BH, Long M. 2013. New genes as drivers of phenotypic evolution. Nat Rev Genet. 14:645-660.
13. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. 2003. DAVID: database for annotation, visualization, integrated discovery. Genome Biol. 4:P3.
14. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15-21.
15. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS. 2003. MicroRNA targets in Drosophila. Genome Biol. 5:R1.
16. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, et al. 2007. High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2:e219.
17. Fay JC, Wu C-I. 2003. Sequence divergence, functional constraint, selection in protein evolution. Annu Rev Genomics Hum Genet. 4:213-235.
18. Friedman RC, Farh KKH, Burge CB, Bartel DP. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19:92-105.
19. Fromm B, Billipp T, Peck LE, Johansen M, Tarver JE, King BL, Newcomb JM, Sempere LF, Flatmark K, Hovig E, et al. 2015. A uniform system for the annotation of vertebrate microRNA genes and the evolution of the human microRNAome. Annu Rev Genet. 49:213-242.
20. Gangaraju VK, Yin H, Weiner MM, Wang J, Huang XA, Lin H. 2011. Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nat Genet. 43:153-158.
21. Ghildiyal M, Zamore PD. 2009. Small silencing RNAs: an expanding universe. Nat Rev Genet. 10:94-108.
22. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF. 2006. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312:75-79.
23. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ. 2006. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34:D140-D144.
24. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. 2008. miRBase: tools for microRNA genomics. Nucleic Acids Res. 36:D154-D158.
25. Guo Z, Maki M, Ding R, Yang Y, Zhang B, Xiong L. 2014. Genome-wide survey of tissue-specific microRNA and transcription factor regulatory networks in 12 tissues. Sci Rep. 4:5150.
26. Haldane JBS. 1933. The part played by recurrent mutation in evolution. Am Nat. 67:5.
27. HanH, ShimH, ShinD, Shim JE, Ko Y, Shin J, KimH, ChoA, KimE, Lee T, et al. 2015. TRRUST: a reference database of human transcriptional regulatory interactions. Sci Rep. 5:11432.
28. Han Y-C, Vidigal JA, Mu P, Yao E, Singh I, Gonz-alez AJ, Concepcion CP, Bonetti C, Ogrodowski P, Carver B, et al. 2015. An allelic series of miR-17-92-mutant mice uncovers functional specialization and cooperation among members of a microRNA polycistron. Nat Genet. 47:766-775.
29. Herranz H, Cohen SM. 2010. MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev. 24:1339-1344.
30. Hornstein E, Shomron N. 2006. Canalization of development by microRNAs. Nat Genet. 38(Suppl):S20-S24.
31. Jacob F, Perrin D, Sanchez C, Monod J. 1960. Operon: a group of genes with the expression coordinated by an operator. C R Hebd Seances Acad Sci. 250:1727-1729.
32. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. 2004. Human microRNA targets. PLoS Biol 2:e363.
33. Kamburov A, Stelzl U, Lehrach H, Herwig R. 2013. The ConsensusPathDB interaction database: 2013 Update. Nucleic Acids Res. 41:D793-D800.
34. Kim VN, Nam JW. 2006. Genomics of microRNA. Trends Genet. 22:165-173.
35. Kim YK, Yu J, Han TS, Park SY, Namkoong B, Kim DH, Hur K, Yoo MW, Lee HJ, Yang HK, et al. 2009. Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res. 37:1672-1681.
36. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16:111-120.
37. Kozomara A, Griffiths-Jones S. 2011. MiRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39:152-157.
38. Kozomara A, Griffiths-Jones S. 2014. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42:D68-D73.
39. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. 2001. Identification of novel genes coding for small expressed RNAs. Science 294:853-858.
40. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T. 2002. Identification of tissue-specific MicroRNAs from mouse. Curr Biol. 12:735-739.
41. Lai EC, Tomancak P, Williams RW, Rubin GM. 2003. Computational identification of Drosophila microRNA genes. Genome Biol. 4:R42.
42. Langfelder P, Horvath S. 2008. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559.
43. Lau NC, Lim LP, Weinstein EG, Bartel DP. 2001. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858-862.
44. Lawrence J. 1999. Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes. Curr Opin Genet Dev. 9:642-648.
45. Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20.
46. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. 2003. Prediction of mammalian MicroRNA targets. Cell 115:787-798.
47. Liang H, Li W-H. 2009. Lowly expressed human microRNA genes evolve rapidly. Mol Biol Evol. 26:1195-1198.
48. Long M, VanKuren NW, Chen S, Vibranovski MD. 2013. New gene evolution: little did we know. Annu Rev Genet. 47:307-333.
49. Lu J, Fu Y, Kumar S, Shen Y, Zeng K, Xu A, Carthew R, Wu C-I. 2008. Adaptive evolution of newly emerged micro-RNA genes in Drosophila. Mol Biol Evol. 25:929-938.
50. Lu J, Shen Y, Carthew RW, Wang SM, Wu C-I. 2010. Reply to evolutionary flux of canonical microRNAs and mirtrons in Drosophila. Nat Genet. 42:9-10.
51. Lu J, Shen Y, WuQ, Kumar S, He B, Shi S, Carthew RW, Wang SM, Wu C-I. 2008. The birth and death of microRNA genes in Drosophila. Nat Genet. 40:351-355.
52. Lyu Y, Shen Y, Li H, Chen Y, Guo L, Zhao Y, Hungate E, Shi S, WuChung ICI, Tang T. 2014. New MicroRNAs in Drosophila-birth, death and cycles of adaptive evolution. PLoS Genet. 10:e1004096.
53. Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, Casillas S, Han Y, Magwire MM, Cridland JM, et al. 2012. The Drosophila melanogaster genetic reference panel. Nature 482:173-178.
54. Mackowiak SD. 2011. Identification of novel and known unit 12. 10 miRNAs in deep-sequencing data with miRDeep2. Curr Protoc Bioinforma 2011:Chapter 12.
55. Marco A, Ninova M, Ronshaugen M, Griffiths-Jones S. 2013. Clusters of microRNAs emerge by new hairpins in existing transcripts. Nucleic Acids Res. 41:7745-7752.
56. Martin M. 2011. Cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet. J. 17:10.
57. Meunier J, Lemoine F, Soumillon M, Liechti A, Weier M, Guschanski K, Hu H, Khaitovich P, Kaessmann H. 2013. Birth and expression evolution of mammalian microRNA genes. Genome Res. 23:34-45.
58. Mogilyansky E, Rigoutsos I. 2013. The miR-17/92 cluster: a comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ. 20:1603-1614.
59. Mohammed J, Bortolamiol-Becet D, Flynt AS, Gronau I, Siepel A, Lai EC. 2014. Adaptive evolution of testis-specific, recently evolved, clustered miRNAs in Drosophila. RNA 20:1195-1209.
60. Mohammed J, Siepel A, Lai EC. 2014. Diverse modes of evolutionary emergence and flux of conserved microRNA clusters. RNA 20:1850-1863.
61. Nielsen R, Hellmann I, Hubisz M, Bustamante C, Clark AG. 2007. Recent and ongoing selection in the human genome. Nat Rev Genet. 8:857-868.
62. Ozsolak F, Poling LL, Wang Z, LiuH, LiuXS, Roeder RG, Zhang X, Song JS, Fisher DE. 2008. Chromatin structure analyses identify miRNA promoters. Genes Dev. 22:3172-3183.
63. Pasquinelli AE, Reinhart BJ, Slack F, MartindaleMQ, Kuroda MI, Maller B, Hayward DC, Ball EE, Degnan B, Müller P, et al. 2000. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408:86-89.
64. Phillips PC. 2008. Epistasis-the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet. 9:855-867.
65. PriceMN, Huang KH, Arkin AP, Alm EJ. 2005. Operon formation is driven by co-regulation and not by horizontal gene transfer. Genome Res. 15:809-819.
66. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-842.
67. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. 2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20:3407-3425.
68. Rajewsky N. 2006. microRNA target predictions in animals. Nat Genet. 38(Suppl):58-513.
69. Roberts A, Pachter L. 2013. Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Methods 10:71-73.
70. Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A. 2004. Identification of mammalian microRNA host genes and transcription units. Genome Res. 14:1902-1910.
71. Ruby JG, Jan CH, Bartel DP. 2007. Intronic microRNA precursors that bypass Drosha processing. Nature 448:83-86.
72. Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC. 2007. Evolution, biogenesis, expression, target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res. 17:1850-1864.
73. Ryazansky SS, Gvozdev VA, Berezikov E. 2011. Evidence for posttranscriptional regulation of clustered microRNAs in Drosophila. BMC Genomics 12:371.
74. Saini HK, Griffiths-Jones S, Enright AJ. 2007. Genomic analysis of human microRNA transcripts. Proc Natl Acad Sci USA. 104:17719-17724.
75. Tarazona S, Garc-a F, Ferrer A, Dopazo J, Conesa A. 2012. NOIseq: a RNAseq differential expression method robust for sequencing depth biases. EMBnetJ. 17:18.
76. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, et al. 2008. Targeted deletion reveals essential and overlapping functions of the miR-17-92 family of miRNA clusters. Cell 132:875-886.
77. Vlachos IS, Zagganas K, ParaskevopoulouMD, Georgakilas G, Karagkouni D, Vergoulis T, Dalamagas T, Hatzigeorgiou AG. 2015. DIANAmiRPath v3. 0: deciphering microRNA function with experimental support. Nucleic Acids Res. 43:W460-W466.
78. Wang J, Haubrock M, Cao K-M, Hua X, Zhang C-Y, Wingender E, Li J. 2011. Regulatory coordination of clustered microRNAs based on microRNA-transcription factor regulatory network. BMC Syst Biol. 5:199.
79. Wang X, Xuan Z, Zhao X, Li Y, ZhangMQ. 2009. High-resolution human core-promoter prediction with CoreBoost-HM. Genome Res. 19:266-275.
80. Yuan X, Liu C, Yang P, He S, Liao Q, Kang S, Zhao Y. 2009. Clustered microRNAs' coordination in regulating protein-protein interaction network. BMC Syst Biol. 3:65.
81. Zhang R, Peng Y, Wang W, Su B. 2007. Rapid evolution of an X-linked microRNA cluster in primates. Genome Res. 17:612-617.
82. Zhang R, Wang Y-Q, Su B. 2008. Molecular evolution of a primatespecific microRNA family. Mol Biol Evol. 25:1493-1502.
83. Zhao H, Zhu L, Zhu Y, Cao J, Li S, Huang Q, Xu T, Huang X, Yan X, Zhu X. 2013. The Cep63 paralogue Deup1 enables massive de novo centriole biogenesis for vertebrate multiciliogenesis. Nat Cell Biol. 15:1434-1444.
84. Zhao W, Langfelder P, Fuller T, Dong J, Li A, Hovarth S. 2010. Weighted gene coexpression network analysis: state of the art. J BiopharmStat. 20:281-300.
85. Zhao Y, Lin J, Xu B, Hu S, Zhang X, Wu L. 2014. MicroRNA-mediated repression of nonsense mRNAs. Elife 8:e03032.