5′ isomiR variation is of functional and evolutionary importance

Nucleic Acids Research

Volumn 42, Issue 14, 2014, Pages 9424-9435

  Tan, Geok Chin ^a,b   Chan, Elcie ^a   Molnar, Attila ^c   Sarkar, Rupa ^a   Alexieva, Diana ^a   Isa, Ihsan Mad ^a   Robinson, Sophie ^a   Zhang, Shuchen ^a   Ellis, Peter ^d   Langford, Cordelia F ^d   Guillot, Pascale V ^a   Chandrashekran, Anil ^a   Fisk, Nick M ^e   Castellano, Leandro ^a   Meister, Gunter ^f,g   Winston, Robert M ^a   Cui, Wei ^a   Baulcombe, David ^c   Dibb, Nick J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^g UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; ARGONAUTE 2 PROTEIN; ARGONAUTE PROTEIN; DNA METHYLTRANSFERASE 3B; MESSENGER RNA; MICRORNA; MICRORNA 302A; MICRORNA 367; MICRORNA 500A; MICRORNA 501; MICRORNA 9; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE 2; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG; UVOMORULIN; RNA PRECURSOR;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FETUS; GENE REPRESSION; GENE SWITCHING; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; ISOMER; LUCIFERASE ASSAY; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; MOLECULAR EVOLUTION; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; RNA SEQUENCE; STRUCTURAL BIOINFORMATICS; ANIMAL; CELL LINE; CHEMISTRY; GENETICS; METABOLISM; STEM CELL;

ANIMALS; ARGONAUTE PROTEINS; CELL LINE; EVOLUTION, MOLECULAR; HUMANS; MICE; MICRORNAS; RNA PRECURSORS; RNA, MESSENGER; STEM CELLS;

EID: 84906283860     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku656     Document Type: Article

References (37)

1. Hamilton, A.J. and Baulcombe, D.C. (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science, 286, 950-952.
2. 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.
3. 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.
4. Kim, V.N. (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat. Rev. Mol. Cell. Biol., 6, 376-385.
5. Ghildiyal, M. and Zamore, P.D. (2009) Small silencing RNAs: an expanding universe. Nat. Rev. Genet., 10, 94-108.
6. Wang, Y., Sheng, G., Juranek, S., Tuschl, T. and Patel, D.J. (2008) Structure of the guide-strand-containing argonaute silencing complex. Nature, 456, 209-213.
7. Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
8. 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.
9. Vasudevan, S., Tong, Y. and Steitz, J.A. (2007) Switching from repression to activation: microRNAs can up-regulate translation. Science, 318, 1931-1934.
10. Orom, U.A., Nielsen, F.C. and Lund, A.H. (2008) MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell, 30, 460-471.
11. Doench, J.G. and Sharp, P.A. (2004) Specificity of microRNA target selection in translational repression. Genes Dev., 18, 504-511.
12. 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.
13. Beitzinger, M., Peters, L., Zhu, J.Y., Kremmer, E. and Meister, G. (2007) Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol., 4, 76-84.
14. Easow, G., Teleman, A.A. and Cohen, S.M. (2007) Isolation of microRNA targets by miRNP immunopurification. RNA, 13, 1198-1204.
15. Karginov, F.V., Conaco, C., Xuan, Z., Schmidt, B.H., Parker, J.S., Mandel, G. and Hannon, G.J. (2007) A biochemical approach to identifying microRNA targets. Proc. Natl. Acad. Sci. U.S.A., 104, 19291-19296.
16. Neilsen, C.T., Goodall, G.J. and Bracken, C.P. (2012) IsomiRs-the overlooked repertoire in the dynamic microRNAome. Trends Genet., 28, 544-549.
17. Morin, R.D., O'Connor, M.D., Griffith, M., Kuchenbauer, F., Delaney, A., Prabhu, A.L., 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.
18. Bartel, D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
19. 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. U.S.A., 105, 7964-7969.
20. Cloonan, N., Wani, S., Xu, Q., Gu, J., Lea, K., Heater, S., Barbacioru, C., Steptoe, A.L., Martin, H.C., Nourbakhsh, E. et al. (2011) MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol., 15, R126.
21. 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. Genes Dev., 24, 992-1009.
22. Fukunaga, R., Han, B.W., Hung, J.H., Xu, J., Weng, Z. and Zamore, P.D. (2012) Dicer partner proteins tune the length of mature miRNAs in flies and mammals. Cell, 151, 533-546.
23. Humphreys, D.T., Hynes, C.J., Patel, H.R., Wei, G.H., Cannon, L., Fatkin, D., Suter, C.M., Clancy, J.L. and Preiss, T. (2012) Complexity of murine cardiomyocyte miRNA biogenesis, sequence variant expression and function. PLoS ONE, 7, e30933.
24. Miska, E.A., Alvarez-Saavedra, E., Abbott, A.L., Lau, N.C., Hellman, A.B., McGonagle, S.M., Bartel, D.P., Ambros, V.R. and Horvitz, H.R. (2007) Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet, 3, e215.
25. Molnar, A., Schwach, F., Studholme, D.J., Thuenemann, E.C. and Baulcombe, D.C. (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature, 447, 1126-1129.
26. Gerrard, L., Rodgers, L. and Cui, W. (2005) Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells, 23, 1234-1241.
27. Ma, L., Young, J., Prabhala, H., Pan, E., Mestdagh, P., Muth, D., Teruya-Feldstein, J., Reinhardt, F., Onder, T.T., Valastyan, S. et al. (2010) miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol., 12, 247-256.
28. Berezikov, E. (2013) Evolution of microRNA diversity and regulation in animals. Nat. Rev. Genet., 12, 846-860.
29. Cho, S., Jang, I., Jun, Y., Yoon, S., Ko, M., Kwon, Y., Choi, I., Chang, H., Ryu, D., Lee, B. et al. (2013) MiRGator v3.0: a microRNA portal for deep sequencing, expression profiling and mRNA targeting. Nucleic Acids Res., 41, D252-D257.
30. Kozomara, A. and Griffiths-Jones, S. (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res., 39, D152-D157.
31. Marco, A., Hui, J.H., Ronshaugen, M. and Griffiths-Jones, S. (2010) Functional shifts in insect microRNA evolution. Genome Biol. Evol., 2, 686-696.
32. 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.
33. Burroughs, A.M., Ando, Y., de Hoon, M.J., Tomaru, Y., Suzuki, H., Hayashizaki, Y. and Daub, C.O. (2010) Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol., 8, 158-177.
34. Fernandez-Valverde, S.L., Taft, R.J. and Mattick, J.S. (2010) Dynamic isomiR regulation in Drosophila development. RNA, 16, 1881-1888.
35. 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.
36. Chen, K. and Rajewsky, N. (2007) The evolution of gene regulation by transcription factors and microRNAs. Nat. Rev. Genet., 8, 93-103.
37. Llorens, F., Banez-Coronel, M., Pantano, L., Del Rio, J.A., Ferrer, I., Estivill, X. and Marti, E. (2013) A highly expressed miR-101 isomiR is a functional silencing small RNA. BMC Genom., 14, 104-121.