Those interfering little RNAs! Silencing and eliminating chromatin

Current Opinion in Genetics and Development

Volumn 14, Issue 2, 2004, Pages 174-180

  Schramke, Vera ^a   Allshire, Robin ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

5 methyl cytosine; 5MeC; Double stranded RNA; dsRNA; Heterochromatin protein 1; Histone H3 methylated on lysine 9; HP1; IESs; Internal eliminated sequences; K9MeH3; Long terminal repeat; LTR; MAC; Macronucleus; MIC; Micronucleus; PKR; Protein kinase dsRNA dependent

Indexed keywords

DNA; DOUBLE STRANDED RNA; INTERFERON; RNA; UNTRANSLATED RNA;

CENTROMERE; CHROMATID ABERRATION; CHROMATIN STRUCTURE; CHROMOSOME SEGREGATION; DNA SEQUENCE; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; HETEROCHROMATIN; METAZOON; NONHUMAN; PHENOTYPE; PLANT GENETICS; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEIN NUCLEIC ACID INTERACTION; PROTEIN RNA BINDING; REVIEW; RNA DEGRADATION; RNA INTERFERENCE; RNA SEQUENCE; RNA TRANSCRIPTION; SEQUENCE HOMOLOGY; SILENCER ELEMENT; TRANSPOSON; YEAST CELL;

ANIMALS; CHROMATIN; DNA TRANSPOSABLE ELEMENTS; GENE SILENCING; INTERFERONS; NUCLEOSOMES; PLANTS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TETRAHYMENA THERMOPHILA;

METAZOA; MYCOBACTERIUM AVIUM COMPLEX (MAC); SCHIZOSACCHAROMYCES POMBE; TRANSPOSONS;

EID: 1942471652     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2004.02.006     Document Type: Review

References (55)

1. Avner P., Heard E. X-chromosome inactivation: counting, choice and initiation. Nat Rev Genet. 2:2001;59-67.
2. Denli A.M., Hannon G.J. RNAi: an ever-growing puzzle. Trends Biochem Sci. 28:2003;196-201.
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. 409:2001;363-366.
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. 293:2001;1146-1150.
5. Vaistij F.E., Jones L., Baulcombe D.C. Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell. 14:2002;857-867.
6. McManus M.T., Sharp P.A. Gene silencing in mammals by small interfering RNAs. Nat Rev Genet. 3:2002;737-747.
7. •].
8. •] show that siRNAs, widely used to knock-down genes, whether chemically synthesised or transcribed from vectors, can induce a non-specific interferon response in mammalian cells.
9. Vaucheret H., Beclin C., Fagard M. Post-transcriptional gene silencing in plants. J Cell Sci. 114:2001;3083-3091.
10. Jones L., Hamilton A.J., Voinnet O., Thomas C.L., Maule A.J., Baulcombe D.C. RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell. 11:1999;2291-2301.
11. Mette M.F., Aufsatz W., van der Winden J., Matzke M.A., Matzke A.J. Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J. 19:2000;5194-5201.
12. Vaucheret H., Fagard M. Transcriptional gene silencing in plants: targets, inducers and regulators. Trends Genet. 17:2001;29-35.
13. Morel J.B., Mourrain P., Beclin C., Vaucheret H. DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis. Curr Biol. 10:2000;1591-1594.
14. Jones L., Ratcliff F., Baulcombe D.C. RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr Biol. 11:2001;747-757.
15. Wassenegger M. RNA-directed DNA methylation. Plant Mol Biol. 43:2000;203-220.
16. Aufsatz W., Mette M.F., van der Winden J., Matzke M., Matzke A.J. HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J. 21:2002;6832-6841.
17. Matzke M., Matzke A.J., Kooter J.M. RNA: guiding gene silencing. Science. 293:2001;1080-1083.
18. Fojtova M., Van Houdt H., Depicker A., Kovarik A. Epigenetic switch from posttranscriptional to transcriptional silencing is correlated with promoter hypermethylation. Plant Physiol. 133:2003;1240-1250 This work in tobacco plants shows that with an increasing number of cell cycles, if PTGS over a transcribed region is maintained, it can lead to promoter methylation and thus TGS.
19. Volpe T.A., Kidner C., Hall I.M., Teng G., Grewal S.I., Martienssen R.A. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science. 297:2002;1833-1837 This seminal study provided the first demonstration that RNAi is involved in the assembly of silent chromatin over specific sequences, fission yeast centromeres in this case. Fission yeast centromeres are transcribed. The resulting transcripts, as well as the conserved components of the RNAi machinery are necessary for the assembly of silent centromeric chromatin by methylation of lysine 9 of histone H3 and recruitment of the HP1 homologue Swi6.
20. Martienssen R.A., Colot V. DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science. 293:2001;1070-1074.
21. Tabara H., Sarkissian M., Kelly W.G., Fleenor J., Grishok A., Timmons L., Fire A., Mello C.C. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell. 99:1999;123-132.
22. Ketting R.F., Haverkamp T.H., van Luenen H.G., Plasterk R.H. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell. 99:1999;133-141.
23. Wu-Scharf D., Jeong B., Zhang C., Cerutti H. Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-box RNA helicase. Science. 290:2000;1159-1162.
24. Vastenhouw N.L., Fischer S.E., Robert V.J., Thijssen K.L., Fraser A.G., Kamath R.S., Ahringer J., Plasterk R.H. A genome-wide screen identifies 27 genes involved in transposon silencing in C. elegans. Curr Biol. 13:2003;1311-1316 This report identifies new factors involved in transposon silencing in C. elegans, providing new hints to understand the mechanism of transposon silencing in greater detail.
25. Sijen T., Plasterk R.H. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature. 426:2003;310-314 This detailed study investigates transposon silencing in C. elegans germline, showing that dsRNA from Tc1 sequences forms dsRNA that effectively silences transposase gene expression through a PTGS-like mechanism. It also gives several insights in the mechanism of RNAi in C. elegans, providing evidence that the dsRNA is edited and spliced.
26. Gendrel A.V., Lippman Z., Yordan C., Colot V., Martienssen R.A. Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science. 297:2002;1871-1873.
27. Llave C., Xie Z., Kasschau K.D., Carrington J.C. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science. 297:2002;2053-2056.
28. Hamilton A., Voinnet O., Chappell L., Baulcombe D. Two classes of short interfering RNA in RNA silencing. EMBO J. 21:2002;4671-4679.
29. Zilberman D., Cao X., Jacobsen S.E. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science. 299:2003;716-719 The authors investigate the Arabidiopsis ARGONAUTE4 mutant. Their study demonstrates a direct link between RNAi and chromatin/DNA methylation. It shows that AGO4 is involved in the locus-specific regulation of the SUPERMAN gene via H3-K9 and DNA methylation. AGO4 is also involved in the formation of silent chromatin on and the accumulation of siRNAs from the AtSN1 retroelement.
30. Aravin A.A., Naumova N.M., Tulin A.V., Vagin V.V., Rozovsky Y.M., Gvozdev V.A. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol. 11:2001;1017-1027.
31. Malinsky S., Bucheton A., Busseau I. New insights on homology-dependent silencing of I factor activity by transgenes containing ORF1 in Drosophila melanogaster. Genetics. 156:2000;1147-1155.
32. Chaboissier M.C., Bucheton A., Finnegan D.J. Copy number control of a transposable element the I factor, a LINE-like element in Drosophila. Proc Natl Acad Sci USA. 95:1998;11781-11785.
33. Schramke V., Allshire R. Hairpin RNAs and retrotransposon LTRs effect RNAi and chromatin-based gene silencing. Science. 301:2003;1069-1074 In this important study the authors show that, in fission yeast, the expression of a synthetic hairpin RNA homologous to a euchromatic gene is sufficient to induce production of homologous siRNAs and the assembly of silent chromatin over the target locus. Therefore no 'magic' cis-acting sequences are required to assemble heterochromatin. In addition, the authors demonstrate that retrotransposon LTRs are silenced by an RNAi-dependent mechanism and act to impose repression on and thus regulate nearby endogenous genes.
34. 6 dispersed SINE repeats elements scattered over the human genome. This study shows that this repetitive elements and others are associated with DNA and K9-H3 methylation.
35. Dawe R.K. RNA interference, transposons, and the centromere. Plant Cell. 15:2003;297-301.
36. Smit A.F., Riggs A.D. Tiggers and DNA transposon fossils in the human genome. Proc Natl Acad Sci USA. 93:1996;1443-1448.
37. Bernard P., Maure J.F., Partridge J.F., Genier S., Javerzat J.P., Allshire R.C. Requirement of heterochromatin for cohesion at centromeres. Science. 294:2001;2539-2542.
38. Reinhart B.J., Bartel D.P. Small RNAs correspond to centromere heterochromatic repeats. Science. 297:2002;1831.
39. Volpe T., Schramke V., Hamilton G.L., White S.A., Teng G., Martienssen R.A., Allshire R.C. RNA interference is required for normal centromere function in fission yeast. Chromosome Res. 11:2003;137-146.
40. Hall I.M., Noma K., Grewal S.I. RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast. Proc Natl Acad Sci USA. 100:2003;193-198.
41. Nakagawa H., Lee J.K., Hurwitz J., Allshire R.C., Nakayama J., Grewal S.I., Tanaka K., Murakami Y. Fission yeast CENP-B homologs nucleate centromeric heterochromatin by promoting heterochromatin-specific histone tail modifications. Genes Dev. 16:2002;1766-1778.
42. Lehnertz B., Ueda Y., Derijck A.A., Braunschweig U., Perez-Burgos L., Kubicek S., Chen T., Li E., Jenuwein T., Peters A.H. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol. 13:2003;1192-1200.
43. Maison C., Bailly D., Peters A.H., Quivy J.P., Roche D., Taddei A., Lachner M., Jenuwein T., Almouzni G. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet. 30:2002;329-334.
44. Yao MC, Yao CH: Genome wide rearrangements of DNA in ciliates. In Mobile DNA II. Edited by N Craig, R Craigie, M Gellert. Washington DC: ASM Press; 2003:730-758.
45. ••].
46. Nikiforov M.A., Gorovsky M.A., Allis C.D. A novel chromodomain protein, pdd3p, associates with internal eliminated sequences during macronuclear development in Tetrahymena thermophila. Mol Cell Biol. 20:2000;4128-4134.
47. Smothers J.F., Mizzen C.A., Tubbert M.M., Cook R.G., Allis C.D. Pdd1p associates with germline-restricted chromatin and a second novel anlagen-enriched protein in developmentally programmed DNA elimination structures. Development. 124:1997;4537-4545.
48. ••].
49. Chalker D.L., Yao M.C. Nongenic, bidirectional transcription precedes and may promote developmental DNA deletion in Tetrahymena thermophila. Genes Dev. 15:2001;1287-1298.
50. ••] this remarkable series of investigations provides direct evidence that dsRNA can target specific sequences (IESs) for deletion in Tetrahymena. These sequences are initially 'marked' by chromatin modifications and an Argonaute homologue is necessary for elimination. These studies lead to a model where sequences due for elimination are packaged in silent chromatin through an RNAi-related mechanism.
51. Bernstein E., Kim S.Y., Carmell M.A., Murchison E.P., Alcorn H., Li M.Z., Mills A.A., Elledge S.J., Anderson K.V., Hannon G.J. Dicer is essential for mouse development. Nat Genet. 35:2003;215-217 This study indicates that Dicer is involved in mouse development because mice born with a homozygous deletion of the Dicer gene die at a very early stage of embryonic development.
52. ••]. This implies that an additional layer of complexity must operate at the silent mating type locus to lock in and maintain the silent state once established via RNAi.
53. Tufarelli C., Stanley J.A., Garrick D., Sharpe J.A., Ayyub H., Wood W.G., Higgs D.R. Transcription of antisense RNA leading to gene silencing and methylation as a novel cause of human genetic disease. Nat Genet. 34:2003;157-165 The authors investigate an inherited form of α-thalassemia in an individual where a deletion brings the LUC7L gene adjacent to the α-globin gene. Despite the presence of all known cis-regulatory elements, the α-globin gene is silenced. The authors develop a transgenic mouse model and show that the expression of an antisense RNA directed from LUC7L into the α-globin gene appears to be responsible for DNA methylation of the α-globin gene CpG island and thus its silencing in both affected individuals and the mouse model.
54. Pal-Bhadra M., Leibovitch B.A., Gandhi S.G., Rao M., Bhadra U., Birchler J.A., Elgin S.C. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science. 303:2004;669-672.
55. Verdel A., Jia S., Gerber S., Sugiyama T., Gygi S., Grewal S.I., Moazed D. RNAi-mediated targeting of heterochromatin by the RITS complex. Science. 303:2004;672-676.