Amplification of siRNA in Caenorhabditis elegans generates a transgenerational sequence-targeted histone H3 lysine 9 methylation footprint

Nature Genetics

Volumn 44, Issue 2, 2012, Pages 157-164

  Gu, Sam Guoping ^a   Pak, Julia ^a   Guang, Shouhong ^b,c   Maniar, Jay M ^a   Kennedy, Scott ^b   Fire, Andrew ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; HISTONE H3; HISTONE H3 LYSINE 9; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CHROMATIN STRUCTURE; CHROMOSOME ANALYSIS; CONTROLLED STUDY; GENE AMPLIFICATION; GENE LOCUS; GENETIC ANALYSIS; HISTONE METHYLATION; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; RNA STABILITY;

ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMATIN; GENE EXPRESSION PROFILING; GENETIC LOCI; HISTONES; LYSINE; METHYLATION; MOLECULAR SEQUENCE DATA; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 84856239588     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.1039     Document Type: Article

References (70)

1. Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811 (1998). (Pubitemid 28099681)
2. Kennerdell, J.R. & Carthew, R.W. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 95, 1017-1026 (1998). (Pubitemid 29019053)
3. Bernstein, E., Caudy, A.A., Hammond, S.M. & Hannon, G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366 (2001). (Pubitemid 32151243)
4. Hammond, S.M., Boettcher, S., Caudy, A.A., Kobayashi, R. & Hannon, G.J. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293, 1146-1150 (2001). (Pubitemid 32758097)
5. Tuschl, T., Zamore, P.D., Lehmann, R., Bartel, D.P. & Sharp, P.A. Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev. 13, 3191-3197 (1999). (Pubitemid 30030441)
6. Hammond, S.M., Bernstein, E., Beach, D. & Hannon, G.J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404, 293-296 (2000). (Pubitemid 30163547)
7. Elbashir, S.M., Lendeckel, W. & Tuschl, T. RNA interference is mediated by 21-and 22-nucleotide RNAs. Genes Dev. 15, 188-200 (2001). (Pubitemid 32107664)
8. Motamedi, M.R. et al. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119, 789-802 (2004). (Pubitemid 40017686)
9. Pak, J. & Fire, A. Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315, 241-244 (2007). (Pubitemid 46166369)
10. Sijen, T., Steiner, F.A., Thijssen, K.L. & Plasterk, R.H. Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315, 244-247 (2007). (Pubitemid 46166370)
11. Saito, K. & Siomi, M.C. Small RNA-mediated quiescence of transposable elements in animals. Dev. Cell 19, 687-697 (2010).
12. Claycomb, J.M. et al. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 139, 123-134 (2009).
13. Batista, P.J. et al. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol. Cell 31, 67-78 (2008).
14. Gent, J.I. et al. Distinct phases of siRNA synthesis in an endogenous RNAi pathway in C. elegans soma. Mol. Cell 37, 679-689 (2010).
15. Maniar, J.M. & Fire, A.Z. EGO-1, a C. elegans RdRP, modulates gene expression via production of mRNA-templated short antisense RNAs. Curr. Biol. 21, 449-459 (2011).
16. Wassenegger, M., Heimes, S., Riedel, L. & Sanger, H.L. RNA-directed de novo methylation of genomic sequences in plants. Cell 76, 567-576 (1994). (Pubitemid 24064176)
17. Matzke, M.A., Primig, M., Trnovsky, J. & Matzke, A.J. Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J. 8, 643-649 (1989).
18. Wassenegger, M. RNA-directed DNA methylation. Plant Mol. Biol. 43, 203-220 (2000).
19. Herr, A.J. & Baulcombe, D.C. RNA silencing pathways in plants. Cold Spring Harb. Symp. Quant. Biol. 69, 363-370 (2004). (Pubitemid 41056574)
20. Volpe, T.A. et al. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833-1837 (2002). (Pubitemid 35024336)
21. Grewal, S.I. RNAi-dependent formation of heterochromatin and its diverse functions. Curr. Opin. Genet. Dev. 20, 134-141 (2010).
22. Moazed, D. Small RNAs in transcriptional gene silencing and genome defence. Nature 457, 413-420 (2009).
23. Mellone, B.G. et al. Centromere silencing and function in fission yeast is governed by the amino terminus of histone H3. Curr. Biol. 13, 1748-1757 (2003). (Pubitemid 37269116)
24. Peters, A.H. et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12, 1577-1589 (2003). (Pubitemid 38037024)
25. Snowden, A.W., Gregory, P.D., Case, C.C. & Pabo, C.O. Gene-specific targeting of H3K9 methylation is sufficient for initiating repression in vivo. Curr. Biol. 12, 2159-2166 (2002). (Pubitemid 36021896)
26. Bannister, A.J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124 (2001). (Pubitemid 32225848)
27. Bühler, M., Verdel, A. & Moazed, D. Tethering RITS to a nascent transcript initiates RNAi-and heterochromatin-dependent gene silencing. Cell 125, 873-886 (2006). (Pubitemid 43795192)
28. Simmer, F. et al. Hairpin RNA induces secondary small interfering RNA synthesis and silencing in trans in fission yeast. EMBO Rep. 11, 112-118 (2010).
29. Simmer, F. et al. Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr. Biol. 12, 1317-1319 (2002). (Pubitemid 34869882)
30. Iida, T., Nakayama, J. & Moazed, D. siRNA-mediated heterochromatin establishment requires HP1 and is associated with antisense transcription. Mol. Cell 31, 178-189 (2008). (Pubitemid 352001402)
31. Aronica, L. et al. Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA elimination in Tetrahymena. Genes Dev. 22, 2228-2241 (2008).
32. Malone, C.D., Anderson, A.M., Motl, J.A., Rexer, C.H. & Chalker, D.L. Germ line transcripts are processed by a Dicer-like protein that is essential for developmentally programmed genome rearrangements of Tetrahymena thermophila. Mol. Cell. Biol. 25, 9151-9164 (2005). (Pubitemid 41429102)
33. Nowacki, M. et al. RNA-mediated epigenetic programming of a genome-rearrangement pathway. Nature 451, 153-158 (2008).
34. Pal-Bhadra, M. et al. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303, 669-672 (2004). (Pubitemid 38141632)
35. Deshpande, G., Calhoun, G. & Schedl, P. Drosophila argonaute-2 is required early in embryogenesis for the assembly of centric/centromeric heterochromatin, nuclear division, nuclear migration, and germ-cell formation. Genes Dev. 19, 1680-1685 (2005). (Pubitemid 41058363)
36. Kanellopoulou, C. et al. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19, 489-501 (2005). (Pubitemid 40256280)
37. Taira, K. Induction of DNA methylation and gene silencing by short interfering RNAs in human cells (Retraction). Nature 441, 1176 (2006).
38. Weinberg, M.S., Barichievy, S., Schaffer, L., Han, J. & Morris, K.V. An RNA targeted to the HIV-1 LTR promoter modulates indiscriminate off-target gene activation. Nucleic Acids Res. 35, 7303-7312 (2007).
39. Morris, K.V., Chan, S.W., Jacobsen, S.E. & Looney, D.J. Small interfering RNA-induced transcriptional gene silencing in human cells. Science 305, 1289-1292 (2004). (Pubitemid 39129233)
40. Kim, D.H., Villeneuve, L.M., Morris, K.V. & Rossi, J.J. Argonaute-1 directs siRNA-mediated transcriptional gene silencing in human cells. Nat. Struct. Mol. Biol. 13, 793-797 (2006). (Pubitemid 44338773)
41. Weinberg, M.S. et al. The antisense strand of small interfering RNAs directs histone methylation and transcriptional gene silencing in human cells. RNA 12, 256-262 (2006). (Pubitemid 43121930)
42. Timmons, L. & Fire, A. Specific interference by ingested dsRNA. Nature 395, 854 (1998).
43. Tabara, H., Grishok, A. & Mello, C.C. RNAi in C. elegans: soaking in the genome sequence. Science 282, 430-431 (1998). (Pubitemid 28483660)
44. Guang, S. et al. Small regulatory RNAs inhibit RNA polymerase II during the elongation phase of transcription. Nature 465, 1097-1101 (2010).
45. Guang, S. et al. An Argonaute transports siRNAs from the cytoplasm to the nucleus. Science 321, 537-541 (2008).
46. Montgomery, M.K., Xu, S. & Fire, A. RNA as a target of double-stranded RNA-mediated genetic interference in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 95, 15502-15507 (1998). (Pubitemid 29018728)
47. Grishok, A., Sinskey, J.L. & Sharp, P.A. Transcriptional silencing of a transgene by RNAi in the soma of C. elegans. Genes Dev. 19, 683-696 (2005). (Pubitemid 40395080)
48. Gu, S.G. & Fire, A. Partitioning the C. elegans genome by nucleosome modification, occupancy, and positioning. Chromosoma 119, 73-87 (2010).
49. Kennedy, S., Wang, D. & Ruvkun, G. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427, 645-649 (2004). (Pubitemid 38248485)
50. Dufourcq, P. et al. lir-2, lir-1 and lin-26 encode a new class of zinc-finger proteins and are organized in two overlapping operons both in Caenorhabditis elegans and in Caenorhabditis briggsae. Genetics 152, 221-235 (1999).
51. Smardon, A. et al. EGO-1 is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans. Curr. Biol. 10, 169-178 (2000). (Pubitemid 30146781)
52. Hodgkin, J., Papp, A., Pulak, R., Ambros, V. & Anderson, P. A new kind of informational suppression in the nematode Caenorhabditis elegans. Genetics 123, 301-313 (1989). (Pubitemid 19248674)
53. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
54. Sijen, T. et al. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107, 465-476 (2001). (Pubitemid 33152782)
55. Alcazar, R.M., Lin, R. & Fire, A.Z. Transmission dynamics of heritable silencing induced by double-stranded RNA in Caenorhabditis elegans. Genetics 180, 1275-1288 (2008).
56. Yigit, E. et al. Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127, 747-757 (2006). (Pubitemid 44716250)
57. Grishok, A., Tabara, H. & Mello, C.C. Genetic requirements for inheritance of RNAi in C. elegans. Science 287, 2494-2497 (2000). (Pubitemid 30185446)
58. Vastenhouw, N.L. et al. Gene expression: long-term gene silencing by RNAi. Nature 442, 882 (2006). (Pubitemid 44285937)
59. Hamilton, A.J. & Baulcombe, D.C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950-952 (1999).
60. Dalmay, T., Hamilton, A., Rudd, S., Angell, S. & Baulcombe, D.C. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101, 543-553 (2000).
61. Mourrain, P. et al. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101, 533-542 (2000).
62. Tabara, H., Yigit, E., Siomi, H. & Mello, C.C. The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans. Cell 109, 861-871 (2002). (Pubitemid 34786001)
63. Tabara, H. et al. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99, 123-132 (1999). (Pubitemid 29491779)
64. Austin, J. & Kimble, J. glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51, 589-599 (1987).
65. Beanan, M.J. & Strome, S. Characterization of a germ-line proliferation mutation in C. elegans. Development 116, 755-766 (1992).
66. Harris, T.W. et al. WormBase: a comprehensive resource for nematode research. Nucleic Acids Res. 38, D463-D467 (2010).
67. Kamath, R.S. et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237 (2003). (Pubitemid 36139121)
68. Timmons, L., Court, D.L. & Fire, A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112 (2001). (Pubitemid 32167059)
69. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
70. Gent, J.I. et al. A Caenorhabditis elegans RNA-directed RNA polymerase in sperm development and endogenous RNA interference. Genetics 183, 1297-1314 (2009).