A meta-Analysis revealed insights into the sources, conservation and impact of microRNA 5′-isoforms in four model species

Nucleic Acids Research

Volumn 42, Issue 3, 2014, Pages 1427-1441

  Xia, Jing ^a,b   Zhang, Weixiong ^a,b,c  

^a JIANGHAN UNIVERSITY   (China)

^b WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' ISOMIR; MESSENGER RNA; MICRORNA; RNA ISOFORM; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENETIC CONSERVATION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PSORIASIS; RNA STRUCTURE; SPECIES DIFFERENCE; STATISTICAL ANALYSIS; TISSUE SPECIFICITY; WORM;

ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MICE; MICRORNAS; MODELS, ANIMAL; PSORIASIS; RNA ISOFORMS; SEQUENCE ANALYSIS, RNA; SKIN;

EID: 84896720225     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt967     Document Type: Article

References (70)

1. Carthew, R.W. and Sontheimer, E.J. (2009) Origins and mechanisms of miRNAs and siRNAs. Cell, 136, 642-655.
2. Bartel, D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
3. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A.O., Landthaler, M. et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell, 129, 1401-1414.
4. 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 21URNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell, 127, 1193-1207.
5. Morin, R.D., Connor, M.D.O., Griffith, M., Kuchenbauer, F., Delaney, A., Prabhu, A., Zhao, Y., Mcdonald, H., Zeng, T., Hirst, M. et al. (2008) Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res., 18, 610-621.
6. Azuma-Mukai, A., Oguri, H., Mituyama, T., Qian, Z.R., Asai, K., Siomi, H. and Siomi, M.C. (2008) Characterization of endogenous human Argonautes and their miRNA partners in RNA silencing. Proc. Natl Acad. Sci., 105, 7964-7969.
7. Berezikov, E., Robine, N., Samsonova, A., Westholm, J.O., Naqvi, A., Hung, J., 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.
8. Chiang, H.R., Schoenfeld, L.W., Ruby, J.G., Auyeung, V.C., Spies, N., Baek, D., Johnston, W.K., Russ, C., Luo, S., Babiarz, J.E. et al. (2010) Mammalian microRNAs : experimental evaluation of novel and previously annotated genes. Gene. Dev., 24, 992-1009.
9. Ebhardt, H.A., Tsang, H.H., Dai, D.C., Liu, Y., Bostan, B. and Fahlman, R.P. (2009) Meta-Analysis of small RNA-sequencing errors reveals ubiquitous post-transcriptional RNA modifications. Nucleic Acids Res., 37, 2461-2470.
10. Fernandez-Valverde, S.L., Taft, R.J. and Mattick, J.S. (2010) Dynamic isomiR regulation in Drosophila development. RNA, 16, 1881-1888.
11. Neilsen, C.T., Goodall, G.J. and Bracken, C.P. (2012) IsomiRs the overlooked repertoire in the dynamic microRNAome. Trends Genet. TIG, 28, 544-549.
12. Reese, T.A., Xia, J., Johnson, L.S., Zhou, X., Zhang, W. and Virgin, H.W. (2010) Identification of novel microRNA-like molecules generated from herpesvirus and host tRNA transcripts. J. Virol., 84, 10344-10353.
13. Ruby, J.G., Stark, A., Johnston, W.K., Kellis, M., Bartel, D.P. and Lai, E.C. (2007) Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res., 17, 1850-1864.
14. 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. (2007) Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature, 450, 219-232.
15. Wu, H., Ye, C., Ramirez, D. and Manjunath, N. (2009) Alternative processing of primary microRNA transcripts by Drosha generates 50 end variation of mature microRNA. PLoS ONE, 4, e7566.
16. Xia, J. and Zhang, W. (2012) Noncanonical microRNAs and endogenous siRNAs in lytic infection of murine gammaherpesvirus. PLoS ONE, 7, e47863.
17. Kuchenbauer, F., Morin, R.D., Argiropoulos, B., Petriv, O.I., Griffith, M., Heuser, M., Yung, E., Piper, J., Delaney, A., Prabhu, A.- L. et al. (2008) In-depth characterization of the microRNA transcriptome in a leukemia progression model. Genome Res., 18, 1787-1797.
18. Guo, L., Yang, Q., Lu, J., Li, H., Ge, Q., Gu, W., Bai, Y. and Lu, Z. (2011) A comprehensive survey of miRNA repertoire and 30 addition events in the placentas of patients with pre-eclampsia from high-throughput sequencing. PLoS ONE, 6, e21072.
19. Burroughs, A.M., Ando, Y., de Hoon, M.J.L., Tomaru, Y., Nishibu, T., Ukekawa, R., Funakoshi, T., Kurokawa, T., Suzuki, H., Hayashizaki, Y. et al. (2010) A comprehensive survey of 30 animal miRNA modification events and a possible role for 30 adenylation in modulating miRNA targeting effectiveness. Genome Res., 20, 1398-1410.
20. Wyman, S.K., Knouf, E.C., Parkin, R.K., Fritz, B.R., Lin, D.W., Dennis, L.M., Krouse, M.A., Webster, P.J. and Tewari, M. (2011) Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res., 21, 1450-1461.
21. Guo, H., Ingolia, N.T., Weissman, J.S. and Bartel, D.P. (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature, 466, 835-840.
22. Baek, D., Villen, J., Shin, C., Camargo, F.D., Gygi, S.P. and Bartel, D.P. (2008) The impact of microRNAs on protein output. Nature, 455, 64-71.
23. Fukunaga, R., Han, B., Hung, J.-H., Xu, J., Weng, Z. and Zamore, P. (2012) Dicer partner proteins tune the length of mature miRNAs in flies and mammals. Cell, 151, 533-546.
24. Park, J.-E., Heo, I., Tian, Y., Simanshu, D.K., Chang, H., Jee, D., Patel, D.J. and Kim, V.N. (2011) Dicer recognizes the 50 end of RNA for efficient and accurate processing. Nature, 475, 201-205.
25. Gu, S., Jin, L., Zhang, Y., Huang, Y., Zhang, F., Valdmanis, P.N. and Kay, M.A. (2012) The loop position of shRNAs and premiRNAs is critical for the accuracy of dicer processing in vivo. Cell, 151, 900-911.
26. Cloonan, N., Wani, S., Xu, Q., Gu, J., Lea, K., Heater, S., Barbacioru, C., Steptoe, A., Martin, H., Nourbakhsh, E. et al. (2011) MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol., 12, R126.
27. Ruby, J.G., Jan, C.H. and Bartel, D.P. (2007) Intronic microRNA precursors that bypass Drosha processing. Nature, 448, 83-86.
28. Ender, C., Krek, A., Friedländer, M.R., Beitzinger, M., Weinmann, L., Chen, W., Pfeffer, S., Rajewsky, N. and Meister, G. (2008) A human snoRNA with microRNA-like functions. Mol. Cell, 32, 519-528.
29. Babiarz, J.E., Ruby, J.G., Wang, Y., Bartel, D.P. and Blelloch, R. (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Gene. Dev., 22, 2773-2785.
30. Brameier, M., Herwig, A., Reinhardt, R., Walter, L. and Gruber, J. (2011) Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs. Nucleic Acids Res., 39, 675-686.
31. Xia, J., Joyce, C.E., Bowcock, A.M. and Zhang, W. (2013) Noncanonical microRNAs and endogenous siRNAs in normal and psoriatic human skin. Hum. Mol. Genet., 22, 737-748.
32. Lee, L.W., Zhang, S., Etheridge, A., Ma, L., Martin, D., Galas, D. and Wang, K. (2010) Complexity of the microRNA repertoire revealed by next-generation sequencing. RNA, 16, 2170-2180.
33. Mart?, E., Pantano, L., Bañez-Coronel, M., Llorens, F., Miñones- Moyano, E., Porta, S., Sumoy, L., Ferrer, I. and Estivill, X. (2010) A myriad of miRNA variants in control and Huntington's disease brain regions detected by massively parallel sequencing. Nucleic Acids Res., 38, 7219-7235.
34. Zhou, H., Arcila, M.L., Li, Z., Lee, E.J., Henzler, C., Liu, J., Rana, T.M. and Kosik, K.S. (2012) Deep annotation of mouse iso-miR and iso-moR variation. Nucleic Acids Res., 40, 5864-5875.
35. Joyce, C.E., Zhou, X., Xia, J., Ryan, C., Thrash, B., Menter, A., Zhang, W. and Bowcock, A.M. (2011) Deep sequencing of small RNAs from human skin reveals major alterations in the psoriasis miRNAome. Hum. Mol. Genet., 20, 4025-4040.
36. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
37. Griffiths-Jones, S., Saini, H.K., van Dongen, S. and Enright, A.J. (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res., 36, D154-D158.
38. Ambros, V., Bartel, B., Bartel, D.P., Burge, C.B., Carrington, J.C., Chen, X., Dreyfuss, G., Eddy, S.R., Griffiths-Jones, S.A.M., Marshall, M. et al. (2003) A uniform system for microRNA annotation. RNA, 9, 277-279.
39. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
40. Hofacker, I.L. (2003) Vienna RNA secondary structure server. Nucleic Acids Res., 31, 3429-3431.
41. Meyer, S., Pfaffl, M. and Ulbrich, S. (2010) Normalization strategies for microRNA profiling experiments: a ''normal'' way to a hidden layer of complexity? Biotechnol. Lett., 32, 1777-1788.
42. Zhang, W., Gao, S., Zhou, X., Xia, J., Chellappan, P., Zhou, X., Zhang, X. and Jin, H. (2010) Multiple distinct small RNAs originate from the same microRNA precursors. Genome Biol., 11, R81.
43. Zhang, X., Xia, J., Lii, Y., Barrera-Figueroa, B., Zhou, X., Gao, S., Lu, L., Niu, D., Chen, Z., Leung, C. et al. (2012) Genome-wide analysis of plant nat-siRNAs reveals insights into their distribution, biogenesis and function. Genome Biol., 13, R20.
44. Friedman, R.C., Farh, K.K., Burge, C.B. and Bartel, D.P. (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res., 19, 92-105.
45. Enright, A., John, B., Gaul, U., Tuschl, T., Sander, C. and Marks, D. (2003) MicroRNA targets in Drosophila. Genome Biol., 5, R1.
46. Mildner, A., Chapnik, E., Manor, O., Yona, S., Kim, K.-W., Aychek, T., Varol, D., Beck, G., Itzhaki, Z.B., Feldmesser, E. et al. (2013) Mononuclear phagocyte miRNome analysis identifies miR- 142 as critical regulator of murine dendritic cell homeostasis. Blood, 121, 1016-1027.
47. Nair, R.P., Duffin, K.C., Helms, C., Ding, J., Stuart, P.E., Goldgar, D., Gudjonsson, J.E., Li, Y., Tejasvi, T., Feng, B.-J. et al. (2009) Genome-wide scan reveals association of psoriasis with IL- 23 and NF-kappaB pathways. Nat. Genet., 41, 199-204.
48. Breitling, R., Armengaud, P., Amtmann, A. and Herzyk, P. (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett., 573, 83-92.
49. Huang da, W. (2007) DAVID bioinformatics resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res., 35, W169-W175.
50. Berezikov, E. (2011) Evolution of microRNA diversity and regulation in animals. Nat. Rev. Genet., 12, 846-860.
51. Yang, J.-S. and Lai, E.C. (2011) Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol. Cell, 43, 892-903.
52. Yamane, A., Resch, W., Kuo, N., Kuchen, S., Li, Z., Sun, H., Robbiani, D.F., McBride, K., Nussenzweig, M.C. and Casellas, R. (2011) Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat. Immunol., 12, 62-69.
53. Lena, A.M., Shalom-Feuerstein, R., di Val Cervo, P.R., Aberdam, D., Knight, R.A., Melino, G. and Candi, E. (2008) miR- 203 represses ''stemness'' by repressing DeltaNp63. Cell Death Differ., 15, 1187-1195.
54. Yi, R., Poy, M.N., Stoffel, M. and Fuchs, E. (2008) A skin microRNA promotes differentiation by repressing ''stemness''. Nature, 452, 225-229.
55. Gennarino, V.A., D'Angelo, G., Dharmalingam, G., Fernandez, S., Russolillo, G., Sanges, R., Mutarelli, M., Belcastro, V., Ballabio, A., Verde, P. et al. (2012) Identification of microRNA-regulated gene networks by expression analysis of target genes. Genome Res., 22, 1163-1172.
56. Swindell, W.R., Johnston, A., Carbajal, S., Han, G., Wohn, C., Lu, J., Xing, X., Nair, R.P., Voorhees, J.J., Elder, J.T. et al. (2011) Genome-wide expression profiling of five mouse models identifies similarities and differences with human psoriasis. PLoS ONE, 6, e18266.
57. Gudjonsson, J.E., Ding, J., Johnston, A., Tejasvi, T., Guzman, A.M., Nair, R.P., Voorhees, J.J., Abecasis, G.R. and Elder, J.T. (2010) Assessment of the psoriatic transcriptome in a large sample: additional regulated genes and comparisons with in vitro models. J. Invest. Dermatol., 130, 1829-1840.
58. De Mulder, K. and Berezikov, E. (2010) Tracing the evolution of tissue identity with microRNAs. Genome Biol., 11, 111.
59. Roux, J., Gonzalez-Porta, M. and Robinson-Rechavi, M. (2012) Comparative analysis of human and mouse expression data illuminates tissue-specific evolutionary patterns of miRNAs. Nucleic Acids Res., 40, 5890-5900.
60. Sorefan, K., Pais, H., Hall, A., Kozomara, A., Griffiths-Jones, S., Moulton, V. and Dalmay, T. (2012) Reducing ligation bias of small RNAs in libraries for next generation sequencing. Silence, 3, 4.
61. Zhuang, F., Fuchs, R.T., Sun, Z., Zheng, Y. and Robb, G.B. (2012) Structural bias in T4 RNA ligase-mediated 30-Adapter ligation. Nucleic Acids Res., 40, e54.
62. Bogerd, H.P., Karnowski, H.W., Cai, X., Shin, J., Pohlers, M. and Cullen, B.R. (2010) A mammalian herpesvirus uses noncanonical expression and processing mechanisms to generate viral MicroRNAs. Mol. Cell, 37, 135-142.
63. Chen, C., Ridzon, D.A., Broomer, A.J., Zhou, Z., Lee, D.H., Nguyen, J.T., Barbisin, M., Xu, N.L., Mahuvakar, V.R., Andersen, M.R. et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res., 33, e179.
64. Kramer, M.F. (2011) Stem-loop RT-qPCR for miRNAs. Curr. Protoc. Mol. Biol., 95, 15.10.1-15.10.15.
65. Grimson, A., Srivastava, M., Fahey, B., Woodcroft, B.J., Chiang, H.R., King, N., Degnan, B.M., Rokhsar, D.S. and Bartel, D.P. (2008) Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature, 455, 1193-1197.
66. Wheeler, B.M., Heimberg, A.M., Moy, V.N., Sperling, E.A., Holstein, T.W., Heber, S. and Peterson, K.J. (2009) The deep evolution of metazoan microRNAs. Evol. Dev., 11, 50-68.
67. Macrae, I.J., Zhou, K., Li, F., Repic, A., Brooks, A.N., Cande, W.Z., Adams, P.D. and Doudna, J. (2006) Structural basis for doublestranded RNA processing by Dicer. Science, 311, 195-198.
68. Starega-Roslan, J., Krol, J., Koscianska, E., Kozlowski, P., Szlachcic, W.J., Sobczak, K. and Krzyzosiak, W.J. (2010) Structural basis of microRNA length variety. Nucleic Acids Res., 39, 257-268.
69. Ryan, B.M., Robles, A.I. and Harris, C.C. (2010) Genetic variation in microRNA networks: the implications for cancer research. Nat. Rev. Cancer, 10, 389-402.
70. Wu, H., Neilson, J.R., Kumar, P., Manocha, M., Shankar, P., Sharp, P.A. and Manjunath, N. (2007) miRNA profiling of na?̈ve, effector and memory CD8 T cells. PLoS ONE, 2, e1020.