Genome-wide annotation and analysis of zebra finch microRNA repertoire reveal sex-biased expression

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Luo, Guan Zheng ^a   Hafner, Markus ^b   Shi, Zhimin ^c   Brown, Miguel ^b   Feng, Gui Hai ^a   Tuschl, Thomas ^b   Wang, Xiu Jie ^a   Li, XiaoChing ^c  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b ROCKEFELLER UNIVERSITY   (United States)

^c LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

MiRNAs; Sequence variations; Sex biased miRNA expression; Tissue enriched miRNA expression; Z chromosome; Zebra finch

Indexed keywords

MICRORNA; MICRORNA 2954; UNCLASSIFIED DRUG; URIDINE;

ADULT ANIMAL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENE LOCATION; GENE MAPPING; GENETIC CONSERVATION; GENETIC DATABASE; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GENOME ANALYSIS; GENOME SIZE; HEART; LIVER; MALE; MUSCLE TISSUE; NONHUMAN; NORTHERN BLOTTING; NUCLEIC ACID BASE SUBSTITUTION; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA SEQUENCE; SEX CHROMOSOME; SEX DIFFERENCE; TAENIOPYGIA GUTTATA;

ANIMALS; BASE SEQUENCE; FEMALE; FINCHES; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MALE; MICRORNAS; SEQUENCE ANALYSIS, DNA; SEX FACTORS; VOCALIZATION, ANIMAL;

AVES; PASSERI; TAENIOPYGIA GUTTATA;

EID: 84871511505     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-727     Document Type: Article

References (74)

1. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136(2):215-233. 10.1016/j.cell.2009.01.002, 19167326.
2. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim S, et al. The nuclear RNase III drosha initiates microRNA processing. Nature 2003, 425(6956):415-419. 10.1038/nature01957, 14508493.
3. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R. The microprocessor complex mediates the genesis of microRNAs. Nature 2004, 432(7014):235-240. 10.1038/nature03120, 15531877.
4. Han J, Lee Y, Yeom KH, Kim YK, Jin H, Kim VN. The drosha-DGCR8 complex in primary microRNA processing. Genes Dev 2004, 18(24):3016-3027. 10.1101/gad.1262504, 535913, 15574589.
5. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009, 11(3):228-234. 10.1038/ncb0309-228, 19255566.
6. Lund E, Guttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science 2004, 303(5654):95-98. 10.1126/science.1090599, 14631048.
7. Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 2003, 17(24):3011-3016. 10.1101/gad.1158803, 305252, 14681208.
8. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010, 11(9):597-610.
9. Yang JS, Phillips MD, Betel D, Mu P, Ventura A, Siepel AC, Chen KC, Lai EC. Widespread regulatory activity of vertebrate microRNA* species. RNA 2011, 17(2):312-326. 10.1261/rna.2537911, 3022280, 21177881.
10. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007, 129(7):1401-1414. 10.1016/j.cell.2007.04.040, 2681231, 17604727.
11. Wyman SK, Knouf EC, Parkin RK, Fritz BR, Lin DW, Dennis LM, Krouse MA, Webster PJ, Tewari M. Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res 2011, 21(9):1450-1461. 10.1101/gr.118059.110, 3166830, 21813625.
12. Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, Baek D, Johnston WK, Russ C, Luo S, Babiarz JE, et al. Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev 2010, 24(10):992-1009. 10.1101/gad.1884710, 2867214, 20413612.
13. Burroughs AM, Ando Y, de Hoon MJ, Tomaru Y, Nishibu T, Ukekawa R, Funakoshi T, Kurokawa T, Suzuki H, Hayashizaki Y, et al. A comprehensive survey of 3′ animal miRNA modification events and a possible role for 3′ adenylation in modulating miRNA targeting effectiveness. Genome Res 2010, 20(10):1398-1410. 10.1101/gr.106054.110, 2945189, 20719920.
14. Brodersen P, Voinnet O. Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 2009, 10(2):141-148.
15. Gu S, Jin L, Zhang F, Sarnow P, Kay MA. Biological basis for restriction of microRNA targets to the 3′ untranslated region in mammalian mRNAs. Nat Struct Mol Biol 2009, 16(2):144-150. 10.1038/nsmb.1552, 2713750, 19182800.
16. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jungkamp AC, Munschauer M, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010, 141(1):129-141. 10.1016/j.cell.2010.03.009, 2861495, 20371350.
17. Dannemann M, Nickel B, Lizano E, Burbano HA, Kelso J. Annotation of primate miRNAs by high throughput sequencing of small RNA libraries. BMC Genomics 2012, 13:116. 10.1186/1471-2164-13-116, 3328248, 22453055.
18. Murchison EP, Kheradpour P, Sachidanandam R, Smith C, Hodges E, Xuan Z, Kellis M, Grutzner F, Stark A, Hannon GJ. Conservation of small RNA pathways in platypus. Genome Res 2008, 18(6):995-1004. 10.1101/gr.073056.107, 2413167, 18463306.
19. Rajasethupathy P, Fiumara F, Sheridan R, Betel D, Puthanveettil SV, Russo JJ, Sander C, Tuschl T, Kandel E. Characterization of small RNAs in aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 2009, 63(6):803-817. 10.1016/j.neuron.2009.05.029, 2875683, 19778509.
20. Wan LC, Zhang H, Lu S, Zhang L, Qiu Z, Zhao Y, Zeng QY, Lin J. Transcriptome-wide identification and characterization of miRNAs from pinus densata. BMC Genomics 2012, 13:132. 10.1186/1471-2164-13-132, 3347991, 22480283.
21. Kozomara A, Griffiths-Jones S. MiRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011, 39(Database issue):D152-157. 3013655, 21037258.
22. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009, 19(1):92-105. 2612969, 18955434.
23. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116(2):281-297. 10.1016/S0092-8674(04)00045-5, 14744438.
24. Doupe AJ, Kuhl PK. Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 1999, 22:567-631. 10.1146/annurev.neuro.22.1.567, 10202549.
25. Nottebohm F. The anatomy and timing of vocal learning in birds. The design of animal communication 1999, 63-110. Mass: MIT Press, Cambridge, Hauser MD, Konishi M.
26. Arnold AP, Itoh Y, Melamed E. A bird′s-eye view of sex chromosome dosage compensation. Annu Rev Genomics Hum Genet 2008, 9:109-127. 10.1146/annurev.genom.9.081307.164220, 18489256.
27. Nottebohm F, Arnold AP. Sexual dimorphism in vocal control areas of the songbird brain. Science 1976, 194(4261):211-213. 10.1126/science.959852, 959852.
28. Mooney R. Neural mechanisms for learned birdsong. Learn Mem 2009, 16(11):655-669. 10.1101/lm.1065209, 19850665.
29. Wada K, Howard JT, McConnell P, Whitney O, Lints T, Rivas MV, Horita H, Patterson MA, White SA, Scharff C, et al. A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc Natl Acad Sci USA 2006, 103(41):15212-15217. 10.1073/pnas.0607098103, 1622802, 17018643.
30. Li X, Wang XJ, Tannenhauser J, Podell S, Mukherjee P, Hertel M, Biane J, Masuda S, Nottebohm F, Gaasterland T. Genomic resources for songbird research and their use in characterizing gene expression during brain development. Proc Natl Acad Sci USA 2007, 104(16):6834-6839. 10.1073/pnas.0701619104, 1850020, 17426146.
31. Replogle K, Arnold AP, Ball GF, Band M, Bensch S, Brenowitz EA, Dong S, Drnevich J, Ferris M, George JM, et al. The songbird neurogenomics (SoNG) initiative: community-based tools and strategies for study of brain gene function and evolution. BMC Genomics 2008, 9:131. 10.1186/1471-2164-9-131, 2329646, 18366674.
32. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Kunstner A, Searle S, White S, Vilella AJ, Fairley S, et al. The genome of a songbird. Nature 2010, 464(7289):757-762. 10.1038/nature08819, 3187626, 20360741.
33. Lovell PV, Clayton DF, Replogle KL, Mello CV. Birdsong ″transcriptomics″: neurochemical specializations of the oscine song system. PLoS One 2008, 3(10):e3440. 10.1371/journal.pone.0003440, 2563692, 18941504.
34. Hilliard AT, Miller JE, Fraley ER, Horvath S, White SA. Molecular microcircuitry underlies functional specification in a basal ganglia circuit dedicated to vocal learning. Neuron 2012, 73(3):537-552. 10.1016/j.neuron.2012.01.005, 3278710, 22325205.
35. Gunaratne PH, Lin YC, Benham AL, Drnevich J, Coarfa C, Tennakoon JB, Creighton CJ, Kim JH, Milosavljevic A, Watson M, et al. Song exposure regulates known and novel microRNAs in the zebra finch auditory forebrain. BMC Genomics 2011, 12(1):277. 10.1186/1471-2164-12-277, 3118218, 21627805.
36. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31(13):3406-3415. 10.1093/nar/gkg595, 169194, 12824337.
37. Griffiths-Jones S. The microRNA registry. Nucleic Acids Res 2004, 32(Database issue):D109-111. 308757, 14681370.
38. Glazov EA, Cottee PA, Barris WC, Moore RJ, Dalrymple BP, Tizard ML. A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res 2008, 18(6):957-964. 10.1101/gr.074740.107, 2413163, 18469162.
39. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC. The mirtron pathway generates microRNA-class regulatory RNAs in drosophila. Cell 2007, 130(1):89-100. 10.1016/j.cell.2007.06.028, 2729315, 17599402.
40. Ruby JG, Jan CH, Bartel DP. Intronic microRNA precursors that bypass drosha processing. Nature 2007, 448(7149):83-86. 10.1038/nature05983, 2475599, 17589500.
41. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC. Mammalian mirtron genes. Mol Cell 2007, 28(2):328-336. 10.1016/j.molcel.2007.09.028, 2763384, 17964270.
42. Yang JS, Lai EC. Dicer-independent, Ago2-mediated microRNA biogenesis in vertebrates. Cell Cycle 2010, 9(22):4455-4460. 10.4161/cc.9.22.13958, 3048044, 21088485.
43. Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, Ma E, Mane S, Hannon GJ, Lawson ND, et al. A novel miRNA processing pathway independent of dicer requires Argonaute2 catalytic activity. Science 2010, 328(5986):1694-1698. 10.1126/science.1190809, 3093307, 20448148.
44. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, Ge H, Bartel DP. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. Elegans. Cell 2006, 127(6):1193-1207. 10.1016/j.cell.2006.10.040, 17174894.
45. Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of drosophila microRNAs. Genome Res 2007, 17(12):1850-1864. 10.1101/gr.6597907, 2099593, 17989254.
46. Zhou H, Arcila ML, Li Z, Lee EJ, Henzler C, Liu J, Rana TM, Kosik KS. Deep annotation of mouse iso-miR and iso-moR variation. Nucleic Acids Res 2012, 40(13):5864-5875. 10.1093/nar/gks247, 3401436, 22434881.
47. Yang W, Chendrimada TP, Wang Q, Higuchi M, Seeburg PH, Shiekhattar R, Nishikura K. Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nat Struct Mol Biol 2006, 13(1):13-21. 10.1038/nsmb1041, 2950615, 16369484.
48. Kawahara Y, Zinshteyn B, Sethupathy P, Iizasa H, Hatzigeorgiou AG, Nishikura K. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science 2007, 315(5815):1137-1140. 10.1126/science.1138050, 2953418, 17322061.
49. Alon S, Mor E, Vigneault F, Church GM, Locatelli F, Galeano F, Gallo A, Shomron N, Eisenberg E. Systematic identification of edited microRNAs in the human brain. Genome Res 2012, 22(8):1533-1540. 10.1101/gr.131573.111, 3409266, 22499667.
50. Zhao D, McBride D, Nandi S, McQueen HA, McGrew MJ, Hocking PM, Lewis PD, Sang HM, Clinton M. Somatic sex identity is cell autonomous in the chicken. Nature 2010, 464(7286):237-242. 10.1038/nature08852, 20220842.
51. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120(1):15-20. 10.1016/j.cell.2004.12.035, 15652477.
52. Morin RD, O′Connor MD, Griffith M, Kuchenbauer F, Delaney A, Prabhu AL, Zhao Y, McDonald H, Zeng T, Hirst M, et al. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 2008, 18(4):610-621. 10.1101/gr.7179508, 2279248, 18285502.
53. Marti E, Pantano L, Banez-Coronel M, Llorens F, Minones-Moyano E, Porta S, Sumoy L, Ferrer I, Estivill X. A myriad of miRNA variants in control and Huntington′s disease brain regions detected by massively parallel sequencing. Nucleic Acids Res 2010, 38(20):7219-7235. 10.1093/nar/gkq575, 2978354, 20591823.
54. Berezikov E, Robine N, Samsonova A, Westholm JO, Naqvi A, Hung JH, Okamura K, Dai Q, Bortolamiol-Becet D, Martin R, et al. Deep annotation of drosophila melanogaster microRNAs yields insights into their processing, modification, and emergence. Genome Res 2011, 21(2):203-215. 10.1101/gr.116657.110, 3032924, 21177969.
55. Lee LW, Zhang S, Etheridge A, Ma L, Martin D, Galas D, Wang K. Complexity of the microRNA repertoire revealed by next-generation sequencing. RNA 2010, 16(11):2170-2180. 10.1261/rna.2225110, 2957056, 20876832.
56. Fernandez-Valverde SL, Taft RJ, Mattick JS. Dynamic isomiR regulation in drosophila development. RNA 2010, 16(10):1881-1888. 10.1261/rna.2379610, 2941097, 20805289.
57. Jones MR, Quinton LJ, Blahna MT, Neilson JR, Fu S, Ivanov AR, Wolf DA, Mizgerd JP. Zcchc11-Dependent uridylation of microRNA directs cytokine expression. Nat Cell Biol 2009, 11(9):1157-1163. 10.1038/ncb1931, 2759306, 19701194.
58. Katoh T, Sakaguchi Y, Miyauchi K, Suzuki T, Kashiwabara S, Baba T. Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(a) polymerase GLD-2. Genes Dev 2009, 23(4):433-438. 10.1101/gad.1761509, 2648654, 19240131.
59. Baccarini A, Chauhan H, Gardner TJ, Jayaprakash AD, Sachidanandam R, Brown BD. Kinetic analysis reveals the fate of a microRNA following target regulation in mammalian cells. Curr Biol 21(5):369-376.
60. Birchler JA. Dosage compensation for the birds. Heredity (Edinb) 2009, 102(5):423-424.
61. Baverstock PR, Adams M, Polkinghorne RW, Gelder M. A sex-linked enzyme in birds-Z-chromosome conservation but no dosage compensation. Nature 1982, 296(5859):763-766. 10.1038/296763a0, 7070516.
62. Kuroda Y, Arai N, Arita M, Teranishi M, Hori T, Harata M, Mizuno S. Absence of Z-chromosome inactivation for five genes in male chickens. Chromosome Res 2001, 9(6):457-468. 10.1023/A:1011672227256, 11592480.
63. McQueen HA, McBride D, Miele G, Bird AP, Clinton M. Dosage compensation in birds. Curr Biol 2001, 11(4):253-257. 10.1016/S0960-9822(01)00070-7, 11250153.
64. Ellegren H, Hultin-Rosenberg L, Brunstrom B, Dencker L, Kultima K, Scholz B. Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol 2007, 5:40. 10.1186/1741-7007-5-40, 2099419, 17883843.
65. Itoh Y, Melamed E, Yang X, Kampf K, Wang S, Yehya N, Van Nas A, Replogle K, Band MR, Clayton DF, et al. Dosage compensation is less effective in birds than in mammals. J Biol 2007, 6(1):2. 10.1186/jbiol53, 2373894, 17352797.
66. Itoh Y, Replogle K, Kim YH, Wade J, Clayton DF, Arnold AP. Sex bias and dosage compensation in the zebra finch versus chicken genomes: general and specialized patterns among birds. Genome Res 2010, 20(4):512-518. 10.1101/gr.102343.109, 2847754, 20357053.
67. Mank JE, Ellegren H. All dosage compensation is local: gene-by-gene regulation of sex-biased expression on the chicken Z chromosome. Heredity (Edinb) 2009, 102(3):312-320.
68. Bisoni L, Batlle-Morera L, Bird AP, Suzuki M, McQueen HA. Female-specific hyperacetylation of histone H4 in the chicken Z chromosome. Chromosome Res 2005, 13(2):205-214. 10.1007/s10577-005-1505-4, 15861309.
69. Melamed E, Arnold AP. Regional differences in dosage compensation on the chicken Z chromosome. Genome Biol 2007, 8(9):R202. 10.1186/gb-2007-8-9-r202, 2375040, 17900367.
70. Reiner A, Laverghetta AV, Meade CA, Cuthbertson SL, Bottjer SW. An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch. J Comp Neurol 2004, 469(2):239-261. 10.1002/cne.11012, 14694537.
71. Arnold AP. Sexual differentiation of the zebra finch song system: positive evidence, negative evidence, null hypotheses, and a paradigm shift. J Neurobiol 1997, 33(5):572-584. 10.1002/(SICI)1097-4695(19971105)33:5<572::AID-NEU6>3.0.CO;2-1, 9369460.
72. Tang YP, Peabody C, Tomaszycki ML, Wade J. Sexually dimorphic SCAMP1 expression in the forebrain motor pathway for song production of juvenile zebra finches. Dev Neurobiol 2007, 67(4):474-482. 10.1002/dneu.20354, 2878128, 17443802.
73. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004, 14(6):1188-1190. 10.1101/gr.849004, 419797, 15173120.
74. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262, 11846609.