Small interfering RNA-producing loci in the ancient parasitic eukaryote Trypanosoma brucei

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Tschudi, Christian ^a   Shi, Huafang ^b   Franklin, Joseph B ^b   Ullu, Elisabetta ^b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Argonaute; Convergent transcription unit; Dicer deficient; Inverted repeat; Retrotransposon; siRNA; Trypanosome

Indexed keywords

ARGONAUTE 1 PROTEIN; DICER; RNA; RNA POLYMERASE II; SMALL INTERFERING RNA;

ARTICLE; CELL NUCLEUS; CENTROMERE; CONTROLLED STUDY; CYTOPLASM; GENE LOCUS; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SEQUENCING; INVERTED REPEAT; NONHUMAN; PROTEIN FAMILY; PROTEIN PURIFICATION; PSEUDOGENE; RETROPOSON; RNA BINDING; RNA SYNTHESIS; TRYPANOSOMA; TRYPANOSOMA BRUCEI; WILD TYPE;

ARGONAUTE PROTEINS; GENETIC LOCI; INVERTED REPEAT SEQUENCES; PROTOZOAN PROTEINS; RETROELEMENTS; RIBONUCLEASE III; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRYPANOSOMA BRUCEI BRUCEI;

EUKARYOTA; TRYPANOSOMA BRUCEI;

EID: 84865324373     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-427     Document Type: Article

References (51)

1. Plasterk RH. RNA silencing: the genome's immune system. Science 2002, 296:1263-1265. 10.1126/science.1072148, 12016302.
2. Girard A, Hannon GJ. Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 2008, 18:136-148. 10.1016/j.tcb.2008.01.004, 2995447, 18282709.
3. Ketting RF. The many faces of RNAi. Dev Cell 2011, 20:148-161. 10.1016/j.devcel.2011.01.012, 21316584.
4. Okamura K, Chung WJ, Ruby JG, Guo H, Bartel DP, Lai EC. The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 2008, 453:803-806. 10.1038/nature07015, 2735555, 18463630.
5. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 2006, 20:3407-3425. 10.1101/gad.1476406, 1698448, 17182867.
6. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, Obata Y, Chiba H, Kohara Y, Kono T, Nakano T, et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008, 453:539-543. 10.1038/nature06908, 18404146.
7. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, Hannon GJ. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453:534-538. 10.1038/nature06904, 2981145, 18404147.
8. Ender C, Krek A, Friedlander MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G. A human snoRNA with microRNA-like functions. Mol Cell 2008, 32:519-528. 10.1016/j.molcel.2008.10.017, 19026782.
9. Cole C, Sobala A, Lu C, Thatcher SR, Bowman A, Brown JW, Green PJ, Barton GJ, Hutvagner G. Filtering of deep sequencing data reveals the existence of abundant dicer-dependent small RNAs derived from tRNAs. RNA 2009, 15:2147-2160. 10.1261/rna.1738409, 2779667, 19850906.
10. Taft RJ, Glazov EA, Lassmann T, Hayashizaki Y, Carninci P, Mattick JS. Small RNAs derived from snoRNAs. RNA 2009, 15:1233-1240. 10.1261/rna.1528909, 2704076, 19474147.
11. Lee YS, Shibata Y, Malhotra A, Dutta A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 2009, 23:2639-2649. 10.1101/gad.1837609, 2779758, 19933153.
12. Haussecker D, Huang Y, Lau A, Parameswaran P, Fire AZ, Kay MA. Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA 2010, 16:673-695. 10.1261/rna.2000810, 2844617, 20181738.
13. Jinek M, Doudna JA. A three-dimensional view of the molecular machinery of RNA interference. Nature 2009, 457:405-412. 10.1038/nature07755, 19158786.
14. Czech B, Hannon GJ. Small RNA sorting: matchmaking for argonautes. Nat Rev Genet 2011, 12:19-31.
15. Ngo H, Tschudi C, Gull K, Ullu E. Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc Natl Acad Sci USA 1998, 95:14687-14692. 10.1073/pnas.95.25.14687, 24510, 9843950.
16. Shi H, Tschudi C, Ullu E. An unusual dicer-like1 protein fuels the RNA interference pathway in Trypanosoma brucei. RNA 2006, 12:2063-2072. 10.1261/rna.246906, 1664728, 17053086.
17. Patrick KL, Shi H, Kolev NG, Ersfeld K, Tschudi C, Ullu E. 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 2009, 106:17933-17938. 10.1073/pnas.0907766106, 2764927, 19815526.
18. Shi H, Ullu E, Tschudi C. Function of the trypanosome argonaute 1 protein in RNA interference requires the N-terminal RGG domain and arginine 735 in the piwi domain. J Biol Chem 2004, 279:49889-49893. 10.1074/jbc.M409280200, 15383544.
19. Shi H, Chamond N, Djikeng A, Tschudi C, Ullu E. RNA interference in Trypanosoma brucei: the role of the amino-terminal RGG domain and the polyribosome association of argonaute1. J Biol Chem 2009, 284:36511-36520. 10.1074/jbc.M109.073072, 2794767, 19880512.
20. Barnes RL, Shi H, Kolev NG, Tschudi C, Ullu E. Comparative genomics reveals two novel RNAi factors in Trypanosoma brucei and provides insight into the core machinery. PLoS Pathog 2012, 8(5):e1002678. 10.1371/journal.ppat.1002678, 3359990, 22654659.
21. Djikeng A, Shi H, Tschudi C, Ullu E. RNA interference in Trypanosoma brucei: cloning of small interfering RNAs provides evidence for retroposon-derived 24-26-nucleotide RNAs. RNA 2001, 7:1522-1530. 1370195, 11720282.
22. Obado SO, Taylor MC, Wilkinson SR, Bromley EV, Kelly JM. Functional mapping of a trypanosome centromere by chromosome fragmentation identifies a 16-kb GC-rich transcriptional "strand-switch" domain as a major feature. Genome Res 2005, 15:36-43. 10.1101/gr.2895105, 540271, 15632088.
23. Shi H, Djikeng A, Tschudi C, Ullu E. Argonaute protein in the early divergent eukaryote Trypanosoma brucei: control of small interfering RNA accumulation and retroposon transcript abundance. Mol Cell Biol 2004, 24:420-427. 10.1128/MCB.24.1.420-427.2004, 303348, 14673174.
24. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, et al. The genome of the African trypanosome Trypanosoma brucei. Science 2005, 309:416-422. 10.1126/science.1112642, 16020726.
25. Ruben L, Egwuagu C, Patton CL. African trypanosomes contain calmodulin which is distinct from host calmodulin. Biochim Biophys Acta 1983, 758:104-113. 10.1016/0304-4165(83)90290-8, 6135450.
26. Hasan G, Turner MJ, Cordingley JS. Complete nucleotide sequence of an unusual mobile element from Trypanosoma brucei. Cell 1984, 37:333-341. 10.1016/0092-8674(84)90329-5, 6327058.
27. Bringaud F, Biteau N, Melville SE, Hez S, El-Sayed NM, Leech V, Berriman M, Neil Hall N, Donelson JE, Baltz T. A new, expressed multigene family containing a hot spot for insertion of retroelements is associated with polymorphic subtelomeric regions of Trypanosoma brucei. Eukaryot Cell 2002, 1:137-151. 10.1128/EC.1.1.137-151.2002, 118050, 12455980.
28. Kimmel BE, Ole-MoiYoi OK, Young JR. Ingi, a 5.2-kb dispersed sequence element from Trypanosoma brucei that carries half of a smaller mobile element at either end and has homology with mammalian LINEs. Mol Cell Biol 1987, 7:1465-1475. 365235, 3037321.
29. Murphy NB, Pays A, Tebabi P, Coquelet H, Guyaux M, Steinert M, Pays E. Trypanosoma brucei repeated element with unusual structural and transcriptional properties. J Mol Biol 1987, 195:855-871. 10.1016/0022-2836(87)90490-6, 3656436.
30. Pays E, Murphy NB. DNA-binding fingers encoded by a trypanosome retroposon. J Mol Biol 1987, 197:147-148. 10.1016/0022-2836(87)90617-6, 2445994.
31. Olivares M, Alonso C, Lopez MC. The open reading frame 1 of the L1Tc retrotransposon of Trypanosoma cruzi codes for a protein with apurinic-apyrimidinic nuclease activity. J Biol Chem 1997, 272:25224-25228. 10.1074/jbc.272.40.25224, 9312137.
32. Aksoy S, Lalor TM, Martin J, Van der Ploeg LH, Richards FF. Multiple copies of a retroposon interrupt spliced leader RNA genes in the African trypanosome, Trypanosoma gambiense. EMBO J 1987, 6:3819-3826. 553854, 2828038.
33. Patrick KL, Luz PM, Ruan JP, Shi H, Ullu E, Tschudi C. Genomic rearrangements and transcriptional analysis of the spliced leader-associated retrotransposon in RNA interference-deficient Trypanosoma brucei. Mol Microbiol 2008, 67:435-447. 2610267, 18067542.
34. White SA, Allshire RC. RNAi-mediated chromatin silencing in fission yeast. Curr Top Microbiol Immunol 2008, 320:157-183. 10.1007/978-3-540-75157-1_8, 18268844.
35. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999, 27:573-580. 10.1093/nar/27.2.573, 148217, 9862982.
36. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009, 10:126-139. 10.1038/nrm2632, 19165215.
37. Okamura K, Balla S, Martin R, Liu N, Lai EC. Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nat Struct Mol Biol 2008, 15:581-590. 10.1038/nsmb.1438, 2713754, 18500351.
38. Warburton PE, Giordano J, Cheung F, Gelfand Y, Benson G. 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 2004, 14:1861-1869. 10.1101/gr.2542904, 524409, 15466286.
39. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
40. Swaminathan J, Baxter EM, Corces VG. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev 2005, 19:65-76. 10.1101/gad.1259105, 540226, 15630020.
41. Dhillon N, Kamakaka RT. A histone variant, Htz1p, and a Sir1p-like protein, Esc2p, mediate silencing at HMR. Mol Cell 2000, 6:769-780. 10.1016/S1097-2765(00)00076-9, 11090616.
42. Lowell JE, Kaiser F, Janzen CJ, Cross GA. Histone H2AZ dimerizes with a novel variant H2B and is enriched at repetitive DNA in Trypanosoma brucei. J Cell Sci 2005, 118:5721-5730. 10.1242/jcs.02688, 16303849.
43. Kato H, Goto DB, Martienssen RA, Urano T, Furukawa K, Murakami Y. RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science 2005, 309:467-469. 10.1126/science.1114955, 15947136.
44. Gordenin DA, Lobachev KS, Degtyareva NP, Malkova AL, Perkins E, Resnick MA. Inverted DNA repeats: a source of eukaryotic genomic instability. Mol Cell Biol 1993, 13:5315-5322. 360228, 8395002.
45. Wen YZ, Zheng LL, Liao JY, Wang MH, Wei Y, Guo XM, Qu LH, Ayala FJ, Lun ZR. Pseudogene-derived small interference RNAs regulate gene expression in African Trypanosoma brucei. Proc Natl Acad Sci USA 2011, 108:8345-8350. 10.1073/pnas.1103894108, 3100955, 21531904.
46. Kolev NG, Franklin JB, Carmi S, Shi H, Michaeli S, Tschudi C. The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog 2010, 6(5):e1001090. 1001010.1001371/journal.ppat.1001090, 2936537, 20838601.
47. Arhin GK, Shen S, Ullu E, Tschudi C. A PCR-based method for gene deletion and protein tagging in Trypanosoma brucei. Methods Mol Biol 2004, 270:277-286.
48. Goecks J, Nekrutenko A, Taylor J. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010, 11:R86. 10.1186/gb-2010-11-8-r86, 2945788, 20738864.
49. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J. Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol 2010, Chapter 19, Supplement 89: Unit 19.10.1-19.10.21.
50. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J, et al. Galaxy: a platform for interactive large-scale genome analysis. Genome Res 2005, 15:1451-1455. 10.1101/gr.4086505, 1240089, 16169926.
51. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.