The structure and repertoire of small interfering RNAs in Leishmania (Viannia) braziliensis reveal diversification in the trypanosomatid RNAi pathway

Molecular Microbiology

Volumn 87, Issue 3, 2013, Pages 580-593

  Atayde, Vanessa D ^a,e   Shi, Huafang ^a   Franklin, Joseph B ^b   Carriero, Nicholas ^c   Notton, Timothy ^d,f   Lye, Lon Fye ^d   Owens, Katherine ^d   Beverley, Stephen M ^d   Tschudi, Christian ^a   Ullu, Elisabetta ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Yale University   (United States)

^d WASHINGTON UNIVERSITY   (United States)

^e MCGILL UNIVERSITY   (Canada)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; DOUBLE STRANDED RNA; HEN1 RNA 2' METHYLTRANSFERASE; PROTOZOAL RNA; RNA METHYLTRANSFERASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; URIDINE;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; GENE LOCUS; GENETIC ASSOCIATION; GENETIC CODE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOME; INVERTED REPEAT; LEISHMANIA BRAZILIENSIS; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PRIORITY JOURNAL; PROTOZOAL GENOME; RNA ANALYSIS; RNA INTERFERENCE; RNA METABOLISM; RNA STRUCTURE; RNA SYNTHESIS; SPECIES COMPARISON; SPECIES DIFFERENCE; TRANSPOSON; TRYPANOSOMA BRUCEI;

ARGONAUTE PROTEINS; GENE EXPRESSION REGULATION; GENETIC VARIATION; LEISHMANIA BRAZILIENSIS; RNA, SMALL INTERFERING; TRYPANOSOMA BRUCEI BRUCEI;

LEISHMANIA BRAZILIENSIS; PROTOZOA; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

EID: 84873059935     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12117     Document Type: Article

References (67)

1. Aksoy, S., Lalor, T.M., Martin, J., Van der Ploeg, L.H., and Richards, F.F. (1987) Multiple copies of a retroposon interrupt spliced leader RNA genes in the African trypanosome, Trypanosoma gambiense. EMBO J 6: 3819-3826.
2. Ameres, S.L., Horwich, M.D., Hung, J.H., Xu, J., Ghildiyal, M., Weng, Z., and Zamore, P.D. (2010) Target RNA-directed trimming and tailing of small silencing RNAs. Science 328: 1534-1539.
3. Aphasizhev, R., Aphasizheva, I., and Simpson, L. (2004) Multiple terminal uridylyltransferases of trypanosomes. FEBS Lett 572: 15-18.
4. Barnes, R.L., Shi, H., Kolev, N.G., Tschudi, C., and Ullu, E. (2012) Comparative genomics reveals two novel RNAi factors in Trypanosoma brucei and provides insight into the core machinery. PLoS Pathog 8: e1002678. doi:1002610.1001371/journal.ppat.1002678
5. Bastin, P., Bagherzadeh, Z., Matthews, K.R., and Gull, K. (1996) A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Mol Biochem Parasitol 77: 235-239.
6. Bazzini, A.A., Lee, M.T., and Giraldez, A.J. (2012) Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336: 233-237.
7. Benson, G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573-580.
8. Boucher, N., Wu, Y., Dumas, C., Dube, M., Sereno, D., Breton, M., and Papadopoulou, B. (2002) A common mechanism of stage-regulated gene expression in Leishmania mediated by a conserved 3′-untranslated region element. J Biol Chem 277: 19511-19520.
9. Bringaud, F., Muller, M., Cerqueira, G.C., Smith, M., Rochette, A., El-Sayed, N.M., etal. (2007) Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog 3: 1291-1307.
10. Bringaud, F., Berriman, M., and Hertz-Fowler, C. (2011) TSIDER1, a short and non-autonomous Salivarian trypanosome-specific retroposon related to the ingi6 subclade. Mol Biochem Parasitol 179: 30-36.
11. Cerutti, H., and Ibrahim, F. (2010) Turnover of mature miRNAs and siRNAs in plants and algae. Adv Exp Med Biol 700: 124-139.
12. Cheloufi, S., Dos Santos, C.O., Chong, M.M., and Hannon, G.J. (2010) A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465: 584-589.
13. Cifuentes, D., Xue, H., Taylor, D.W., Patnode, H., Mishima, Y., Cheloufi, S., etal. (2010) A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science 328: 1694-1698.
14. Cole, C., Sobala, A., Lu, C., Thatcher, S.R., Bowman, A., Brown, J.W., etal. (2009) Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA 15: 2147-2160.
15. Djikeng, A., Shi, H., Tschudi, C., and Ullu, E. (2001) RNA interference in Trypanosoma brucei: cloning of small interfering RNAs provides evidence for retroposon-derived 24-26-nucleotide RNAs. RNA 7: 1522-1530.
16. Djikeng, A., Shi, H., Tschudi, C., Shen, S., and Ullu, E. (2003) An siRNA ribonucleoprotein is found associated with polyribosomes in Trypanosoma brucei. RNA 9: 802-808.
17. Djuranovic, S., Nahvi, A., and Green, R. (2012) miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336: 237-240.
18. Durand-Dubief, M., and Bastin, P. (2003) TbAGO1, an Argonaute protein required for RNA interference, is involved in mitosis and chromosome segregation in Trypanosoma brucei. BMC Biol 1: 2. doi:10.1186/1741-7007-1181-1182
19. Elbashir, S.M., Lendeckel, W., and Tuschl, T. (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15: 188-200.
20. Ender, C., and Meister, G. (2010) Argonaute proteins at a glance. J Cell Sci 123: 1819-1823.
21. Ender, C., Krek, A., Friedlander, M.R., Beitzinger, M., Weinmann, L., Chen, W., etal. (2008) A human snoRNA with microRNA-like functions. Mol Cell 32: 519-528.
22. Fabian, M.R., Sonenberg, N., and Filipowicz, W. (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: 351-379.
23. Fernandes, A.P., Nelson, K., and Beverley, S.M. (1993) Evolution of nuclear ribosomal RNAs in kinetoplastid protozoa: perspectives on the age and origins of parasitism. Proc Natl Acad Sci USA 90: 11608-11612.
24. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E., and Mello, C.C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
25. Fu, G., and Barker, D.C. (1998) Characterisation of Leishmania telomeres reveals unusual telomeric repeats and conserved telomere-associated sequence. Nucleic Acids Res 26: 2161-2167.
26. Fu, G., Perona-Wright, G., and Barker, D.C. (1998) Leishmania braziliensis: characterisation of a complex specific subtelomeric repeat sequence and its use in the detection of parasites. Exp Parasitol 90: 236-243.
27. 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.
28. Hamilton, A.J., and Baulcombe, D.C. (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286: 950-952.
29. Haussecker, D., Huang, Y., Lau, A., Parameswaran, P., Fire, A.Z., and Kay, M.A. (2010) Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA 16: 673-695.
30. Horwich, M.D., Li, C., Matranga, C., Vagin, V., Farley, G., Wang, P., and Zamore, P.D. (2007) The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr Biol 17: 1265-1272.
31. Huang, H.Y., Houwing, S., Kaaij, L.J., Meppelink, A., Redl, S., Gauci, S., etal. (2011) Tdrd1 acts as a molecular scaffold for Piwi proteins and piRNA targets in zebrafish. EMBO J 30: 3298-3308.
32. Ibrahim, F., Rymarquis, L.A., Kim, E.J., Becker, J., Balassa, E., Green, P.J., and Cerutti, H. (2010) Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc Natl Acad Sci USA 107: 3906-3911.
33. Ji, L., and Chen, X. (2012) Regulation of small RNA stability: methylation and beyond. Cell Res 22: 624-636.
34. Kim, V.N., Han, J., and Siomi, M.C. (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139.
35. Kim, Y.K., Heo, I., and Kim, V.N. (2010) Modifications of small RNAs and their associated proteins. Cell 143: 703-709.
36. Kirino, Y., and Mourelatos, Z. (2007) The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs. RNA 13: 1397-1401.
37. Kurth, H.M., and Mochizuki, K. (2009) 2′-O-methylation stabilizes Piwi-associated small RNAs and ensures DNA elimination in Tetrahymena. RNA 15: 675-685.
38. 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.
39. Lee, R.C., Feinbaum, R.L., and Ambros, V. (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854.
40. Lee, Y.S., Shibata, Y., Malhotra, A., and Dutta, A. (2009) A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 23: 2639-2649.
41. Li, J., Yang, Z., Yu, B., Liu, J., and Chen, X. (2005) Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr Biol 15: 1501-1507.
42. Liu, Q., and Paroo, Z. (2010) Biochemical principles of small RNA pathways. Annu Rev Biochem 79: 295-319.
43. van Luenen, H.G., Farris, C., Jan, S., Genest, P.A., Tripathi, P., Velds, A., etal. (2012) Glucosylated hydroxymethyluracil, DNA base J, prevents transcriptional readthrough in Leishmania. Cell 150: 909-921.
44. Lye, L.F., Owens, K., Shi, H., Murta, S.M., Vieira, A.C., Turco, S.J., etal. (2010) Retention and loss of RNA interference pathways in trypanosomatid protozoans. PLoS Pathog 6: e1001161. doi:1001110.1001371/journal.ppat.1001161
45. McNicoll, F., Muller, M., Cloutier, S., Boilard, N., Rochette, A., Dube, M., and Papadopoulou, B. (2005) Distinct 3′-untranslated region elements regulate stage-specific mRNA accumulation and translation in Leishmania. J Biol Chem 280: 35238-35246.
46. 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.
47. Muller, M., Padmanabhan, P.K., Rochette, A., Mukherjee, D., Smith, M., Dumas, C., and Papadopoulou, B. (2010) Rapid decay of unstable Leishmania mRNAs bearing a conserved retroposon signature 3′-UTR motif is initiated by a site-specific endonucleolytic cleavage without prior deadenylation. Nucleic Acids Res 38: 5867-5883.
48. Ngo, H., Tschudi, C., Gull, K., and Ullu, E. (1998) Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc Natl Acad Sci USA 95: 14687-14692.
49. Patrick, K.L., Shi, H., Kolev, N.G., Ersfeld, K., Tschudi, C., and Ullu, E. (2009) Distinct and overlapping roles for two Dicer-like proteins in the RNA interference pathways of the ancient eukaryote Trypanosoma brucei. Proc Natl Acad Sci USA 106: 17933-17938.
50. Peacock, C.S., Seeger, K., Harris, D., Murphy, L., Ruiz, J.C., Quail, M.A., etal. (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39: 839-847.
51. Pelisson, A., Sarot, E., Payen-Groschene, G., and Bucheton, A. (2007) A novel repeat-associated small interfering RNA-mediated silencing pathway downregulates complementary sense gypsy transcripts in somatic cells of the Drosophila ovary. J Virol 81: 1951-1960.
52. Ren, G., Chen, X., and Yu, B. (2012) Uridylation of miRNAs by hen1 suppressor1 in Arabidopsis. Curr Biol 22: 695-700.
53. Saito, K., Sakaguchi, Y., Suzuki, T., Siomi, H., and Siomi, M.C. (2007) Pimet, the Drosophila homolog of HEN1, mediates 2′-O-methylation of Piwi-interacting RNAs at their 3′ ends. Genes Dev 21: 1603-1608.
54. Saraiya, A.A., and Wang, C.C. (2008) snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4: e1000224. doi:1000210.1001371/journal.ppat.1000224
55. Shi, H., Djikeng, A., Tschudi, C., and Ullu, E. (2004) Argonaute protein in the early divergent eukaryote Trypanosoma brucei: control of small interfering RNA accumulation and retroposon transcript abundance. Mol Cell Biol 24: 420-427.
56. Shi, H., Tschudi, C., and Ullu, E. (2006) An unusual Dicer-like1 protein fuels the RNA interference pathway in Trypanosoma brucei. RNA 12: 2063-2072.
57. Smith, M., Bringaud, F., and Papadopoulou, B. (2009) Organization and evolution of two SIDER retroposon subfamilies and their impact on the Leishmania genome. BMC Genomics 10: 240.
58. Stagno, J., Aphasizheva, I., Aphasizhev, R., and Luecke, H. (2007) Dual role of the RNA substrate in selectivity and catalysis by terminal uridylyl transferases. Proc Natl Acad Sci USA 104: 14634-14639.
59. Stein, L.D., Mungall, C., Shu, S., Caudy, M., Mangone, M., Day, A., etal. (2002) The generic genome browser: a building block for a model organism system database. Genome Res 12: 1599-1610.
60. Tschudi, C., Shi, H., Franklin, J.B., and Ullu, E. (2012) Small interfering RNA-producing loci in the ancient parasitic eukaryote Trypanosoma brucei. BMC Genomics 13: 427.
61. Warburton, P.E., Giordano, J., Cheung, F., Gelfand, Y., and Benson, G. (2004) Inverted repeat structure of the human genome: the X-chromosome contains a preponderance of large, highly homologous inverted repeats that contain testes genes. Genome Res 14: 1861-1869.
62. Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., etal. (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453: 539-543.
63. Wen, Y.Z., Zheng, L.L., Liao, J.Y., Wang, M.H., Wei, Y., Guo, X.M., etal. (2011) Pseudogene-derived small interference RNAs regulate gene expression in African Trypanosoma brucei. Proc Natl Acad Sci USA 108: 8345-8350.
64. Wightman, B., Ha, I., and Ruvkun, G. (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75: 855-862.
65. van Wolfswinkel, J.C., Claycomb, J.M., Batista, P.J., Mello, C.C., Berezikov, E., and Ketting, R.F. (2009) CDE-1 affects chromosome segregation through uridylation of CSR-1-bound siRNAs. Cell 139: 135-148.
66. Yang, J.S., Maurin, T., Robine, N., Rasmussen, K.D., Jeffrey, K.L., Chandwani, R., etal. (2010) Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc Natl Acad Sci USA 107: 15163-15168.
67. Zhao, Y., Yu, Y., Zhai, J., Ramachandran, V., Dinh, T.T., Meyers, B.C., etal. (2012) The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr Biol 22: 689-694.