The ERI-6/7 helicase acts at the first stage of an siRNA amplification pathway that targets recent gene duplications

PLoS Genetics

Volumn 7, Issue 11, 2011, Pages

  Fischer, Sylvia E J ^a   Montgomery, Taiowa A ^a   Zhang, Chi ^a   Fahlgren, Noah ^b   Breen, Peter C ^a   Hwang, Alexia ^a   Sullivan, Christopher M ^b   Carrington, James C ^b   Ruvkun, Gary ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARMITAGE PROTEIN; DICER; DOUBLE STRANDED RNA; ERGO 1 PROTEIN; ERI 6 PROTEIN; ERI 7 PROTEIN; HELICASE; MOV10 PROTEIN; NUCLEOTIDE; REGULATOR PROTEIN; SDE3 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; ERGO 1 PROTEIN, C ELEGANS; ERGO-1 PROTEIN, C ELEGANS; ERI 6 PROTEIN, C ELEGANS; ERI-6 PROTEIN, C ELEGANS; RIBONUCLEASE III; RNA BINDING PROTEIN;

ARABIDOPSIS; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ERI 6 GENE; ERI 7 GENE; GENE; GENE AMPLIFICATION; GENE DELETION; GENE DUPLICATION; GENE IDENTIFICATION; GENE LOCUS; GENE MUTATION; GENE SILENCING; NONHUMAN; OOCYTE; PROTEIN PROCESSING; PSEUDOGENE; RNA STABILITY; SEQUENCE HOMOLOGY; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION;

ANIMALIA; ARABIDOPSIS; CAENORHABDITIS ELEGANS; FUNGI;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA HELICASES; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENE SILENCING; MUTATION; OOCYTES; PSEUDOGENES; RIBONUCLEASE III; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

EID: 81755177836     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002369     Document Type: Article

References (51)

1. Hamilton A, Voinnet O, Chappell L, Baulcombe D, (2002) Two classes of short interfering RNA in RNA silencing. Embo J 21: 4671-4679.
2. Ambros V, Lee RC, Lavanway A, Williams PT, Jewell D, (2003) MicroRNAs and Other Tiny Endogenous RNAs in C. elegans. Curr Biol 13: 807-818.
3. Okamura K, Chung WJ, Ruby JG, Guo H, Bartel DP, et al. (2008) The Drosophila hairpin RNA pathway generates endogenous short interfering RNAs. Nature 453: 803-806.
4. Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, et al. (2008) An endogenous small interfering RNA pathway in Drosophila. Nature 453: 798-802.
5. Kawamura Y, Saito K, Kin T, Ono Y, Asai K, et al. (2008) Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 453: 793-797.
6. Watanabe T, Totoki Y, Toyoda A, Kaneda M, Kuramochi-Miyagawa S, et al. (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453: 539-543.
7. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, et al. (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453: 534-538.
8. Sijen T, Plasterk RH, (2003) Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 426: 310-314.
9. van Wolfswinkel JC, Claycomb JM, Batista PJ, Mello CC, Berezikov E, et al. (2009) CDE-1 affects chromosome segregation through uridylation of CSR-1-bound siRNAs. Cell 139: 135-148.
10. Claycomb JM, Batista PJ, Pang KM, Gu W, Vasale JJ, et al. (2009) The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 139: 123-134.
11. Zhang C, Montgomery TA, Gabel HW, Fischer SE, Phillips CM, et al. (2011) Inaugural Article: mut-16 and other mutator class genes modulate 22G and 26G siRNA pathways in Caenorhabditis elegans. Proc Natl Acad Sci U S A 108: 1201-1208.
12. Gu W, Shirayama M, Conte D Jr, Vasale J, Batista PJ, et al. (2009) Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol Cell 36: 231-244.
13. Bernstein E, Caudy AA, Hammond SM, Hannon GJ, (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366.
14. Ketting RF, Fischer SE, Bernstein E, Sijen T, Hannon GJ, et al. (2001) Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 15: 2654-2659.
15. Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S, et al. (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107: 465-476.
16. Steiner FA, Okihara KL, Hoogstrate SW, Sijen T, Ketting RF, (2009) RDE-1 slicer activity is required only for passenger-strand cleavage during RNAi in Caenorhabditis elegans. Nat Struct Mol Biol 16: 207-211.
17. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, et al. (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127: 1193-1207.
18. Han T, Manoharan AP, Harkins TT, Bouffard P, Fitzpatrick C, et al. (2009) 26G endo-siRNAs regulate spermatogenic and zygotic gene expression in Caenorhabditis elegans. Proc Natl Acad Sci U S A 106: 18674-18679.
19. Vasale JJ, Gu W, Thivierge C, Batista PJ, Claycomb JM, et al. (2010) Sequential rounds of RNA-dependent RNA transcription drive endogenous small-RNA biogenesis in the ERGO-1/Argonaute pathway. Proc Natl Acad Sci U S A 107: 3582-3587.
20. Conine CC, Batista PJ, Gu W, Claycomb JM, Chaves DA, et al. (2010) Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26G-RNAs and thermotolerant sperm in Caenorhabditis elegans. Proc Natl Acad Sci U S A 107: 3588-3593.
21. Gent JI, Lamm AT, Pavelec DM, Maniar JM, Parameswaran P, et al. (2010) Distinct phases of siRNA synthesis in an endogenous RNAi pathway in C. elegans soma. Mol Cell 37: 679-689.
22. Duchaine TF, Wohlschlegel JA, Kennedy S, Bei Y, Conte D Jr, et al. (2006) Functional proteomics reveals the biochemical niche of C. elegans DCR-1 in multiple small-RNA-mediated pathways. Cell 124: 343-354.
23. Pavelec DM, Lachowiec J, Duchaine TF, Smith HE, Kennedy S, (2009) Requirement for the ERI/DICER complex in endogenous RNA interference and sperm development in Caenorhabditis elegans. Genetics 183: 1283-1295.
24. Welker NC, Pavelec DM, Nix DA, Duchaine TF, Kennedy S, et al. (2010) Dicer's helicase domain is required for accumulation of some, but not all, C. elegans endogenous siRNAs. RNA 16: 893-903.
25. Guang S, Bochner AF, Pavelec DM, Burkhart KB, Harding S, et al. (2008) An Argonaute transports siRNAs from the cytoplasm to the nucleus. Science 321: 537-541.
26. Yigit E, Batista PJ, Bei Y, Pang KM, Chen CC, et al. (2006) Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127: 747-757.
27. Chendrimada TP, Finn KJ, Ji X, Baillat D, Gregory RI, et al. (2007) MicroRNA silencing through RISC recruitment of eIF6. Nature 447: 823-828.
28. Frost RJA, Hamra FK, Richardson JA, Qi X, Bassel-Duby R, et al. (2010) MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwi-interacting RNAs. Proc Natl Acad Sci USA 107: 11847-11852.
29. Fischer SE, Butler MD, Pan Q, Ruvkun G, (2008) Trans-splicing in C. elegans generates the negative RNAi regulator ERI-6/7. Nature 455: 491-496.
30. Matranga C, Tomari Y, Shin C, Bartel DP, Zamore PD, (2005) Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 123: 607-620.
31. Stoeckius M, Maaskola J, Colombo T, Rahn HP, Friedlander MR, et al. (2009) Large-scale sorting of C. elegans embryos reveals the dynamics of small RNA expression. Nature methods 6: 745-751.
32. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330: 1775-1787.
33. Katju V, Lynch M, (2003) The structure and early evolution of recently arisen gene duplicates in the Caenorhabditis elegans genome. Genetics 165: 1793-1803.
34. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, et al. (2003) The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1: e45 doi:10.1371/journal.pbio.0000045.
35. Schrimpf SP, Weiss M, Reiter L, Ahrens CH, Jovanovic M, et al. (2009) Comparative functional analysis of the Caenorhabditis elegans and Drosophila melanogaster proteomes. PLoS Biol 7: e48 10.1371/journal.pbio.1000048.
36. Lynch M, Conery JS, (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
37. Lipinski KJ, Farslow JC, Fitzpatrick KA, Lynch M, Katju V, et al. (2011) High spontaneous rate of gene duplication in Caenorhabditis elegans. Current biology: CB 21: 306-310.
38. Guang S, Bochner AF, Burkhart KB, Burton N, Pavelec DM, et al. (2010) Small regulatory RNAs inhibit RNA polymerase II during the elongation phase of transcription. Nature 465: 1097-1101.
39. Simmer F, Tijsterman M, Parrish S, Koushika SP, Nonet ML, et al. (2002) Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr Biol 12: 1317-1319.
40. Allen E, Xie Z, Gustafson AM, Carrington JC, (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221.
41. Welker NC, Maity TS, Ye X, Aruscavage PJ, Krauchuk AA, et al. (2011) Dicer's helicase domain discriminates dsRNA termini to promote an altered reaction mode. Molecular Cell 41: 589-599.
42. Miyoshi K, Tsukumo H, Nagami T, Siomi H, Siomi MC, (2005) Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev 19: 2837-2848.
43. Rand TA, Petersen S, Du F, Wang X, (2005) Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation. Cell 123: 621-629.
44. Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E, et al. (2010) In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol Cell 39: 282-291.
45. Kennedy S, Wang D, Ruvkun G, (2004) A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427: 645-649.
46. Fischer SE, Wienholds E, Plasterk RH, (2003) Continuous Exchange of Sequence Information Between Dispersed Tc1 Transposons in the Caenorhabditis elegans Genome. Genetics 164: 127-134.
47. Meister G, Landthaler M, Peters L, Chen PY, Urlaub H, et al. (2005) Identification of novel argonaute-associated proteins. Curr Biol 15: 2149-2155.
48. Tomari Y, Du T, Haley B, Schwarz DS, Bennett R, et al. (2004) RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 116: 831-841.
49. Lee RC, Hammell CM, Ambros V, (2006) Interacting endogenous and exogenous RNAi pathways in Caenorhabditis elegans. Rna 12: 589-597.
50. Hoogewijs D, Houthoofd K, Matthijssens F, Vandesompele J, Vanfleteren JR, (2008) Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol Biol 9: 9.
51. Fahlgren N, Sullivan CM, Kasschau KD, Chapman EJ, Cumbie JS, et al. (2009) Computational and analytical framework for small RNA profiling by high-throughput sequencing. RNA 15: 992-1002.