Mechanisms of gene silencing by double-stranded RNA

Nature

Volumn 431, Issue 7006, 2004, Pages 343-349

  Meister, Gunter ^a   Tuschl, Thomas ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GENETIC ENGINEERING; MICROORGANISMS;

GENE EXPRESSION; RNA SILENCING;

RNA;

ADENOSINE DEAMINASE; DOUBLE STRANDED RNA; ENDONUCLEASE; MESSENGER RNA; RIBONUCLEOPROTEIN;

RNA;

AMINO ACID SEQUENCE; ENZYME ACTIVITY; EUKARYOTE; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA CLEAVAGE; RNA EDITING; RNA INTERFERENCE; RNA PROCESSING; RNA STRUCTURE; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; STRUCTURE ANALYSIS;

ANIMALS; GENE SILENCING; PROTEIN BIOSYNTHESIS; RIBONUCLEOPROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, DOUBLE-STRANDED; RNA, MESSENGER;

ARACHNIDA; EUKARYOTA; HEXAPODA;

EID: 4644223259     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature02873     Document Type: Review

References (98)

1. Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811 (1998).
2. Tijsterman, M., Ketting, R. F. & Plasterk, R. H. The genetics of RNA silencing. Annu. Rev. Genet. 36, 489-519 (2002).
3. Ullu, E., Tschudi, C. & Chakraborty, T. RNA interference in protozoan parasites. Cell Microbiol. 6, 509-519 (2004).
4. Waterhouse, P. M., Wang, M. B. & Lough, T. Gene silencing as an adaptive defence against viruses. Nature 411, 834-842 (2001).
5. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
6. Lee, Y., Jeon, K., Lee, J. T., Kim, S. & Kim, V. N. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 21, 4663-4670 (2002).
7. Lee, Y. et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419 (2003).
8. Basyuk, E., Suavet, F., Doglio, A., Bordonne, R. & Bertrand, E. Human let-7 stem-loop precursors harbor features of RNase III cleavage products. Nucleic Acids Res. 31, 6593-6597 (2003).
9. Bohnsack, M. T., Czaplinski, K. & Görlich, D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10, 185-191 (2004).
10. Lund, E., Guttinger, S., Calado, A., Dahlberg, J. E. & Kutay, U. Nuclear export of microRNA precursors. Seience 303, 95-98 (2004).
11. Yi, R., Qin, Y., Macara, I. G. & Cullers, B. R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17, 3011-3016 (2003).
12. Hutvágner, G., McLachlan, J., Bálint, É., Tuschl, T. & Zamore, P. D. A cellular function for the RNA interference enzyme Dicer in small temporal RNA maturation. Science 93, 834-838 (2001).
13. Grishok, A. et al. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106, 23-34 (2001).
14. Lee, Y. S. et al. Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69-81 (2004).
15. Xie, Z. et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104 (2004).
16. Bernstein, E., Gaudy, 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).
17. Elbashir, S. M., Lendeckel, W. & Tuschl, T. RNA interference is mediated by 21 and 22 nt RNAs. Genes Dev. 15, 188-200 (2001).
18. Liu, Q. et al. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301, 1921-1925 (2003).
19. Pham, J. W., Pellino, J. L., Lee, Y. S., Carthew, R. W. & Sontheimer, E. J. A Dicer-2-dependent 80S complex cleaves targeted mRNAs during RNAi in Drosophila. Cell 117, 83-94 (2004).
20. Nykänen, A., Haley, B. & Zamore, P. D. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107, 309-321 (2001).
21. Provost, P. et al. Ribonuclease activity and RNA binding of recombinant human Dicer. EMBO J. 21, 5864-5874 (2002).
22. Zhang, H., Kolb, F. A., Brondani, V., Billy, E. & Filipowicz, W. Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. EMBO J. 21, 5875-5885 (2002).
23. Boutet, S. et al. Arabidopsts HEN1: A genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr. Biol. 13, 843-848 (2003).
24. Vazquez, F., Gasciolli, V., Crete, P. & Vaucheret, H. The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not post-transcriptional transgene silencing. Curr. Biol. 14, 346-351 (2004).
25. Han, M. H., Goud, S., Song, L. & Fedoroff, N. The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc. Natl Acad. Sci. USA 101, 1093-1098 (2004).
26. 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).
27. 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).
28. Mourelatos, Z. et al. miRNPs: a novel class of ribonudeoproteins containing numerous microRNAs. Genes Dev. 16, 720-728 (2002).
29. Hammond, S. M., Boettcher, S., Gaudy, A. A., Kobayashi, R. & Hannon, G. J. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293, 1146-1150 (2001).
30. Martinez, J., Patkaniowska, A., Urlaub, H., Lührmann, R. & Tuschl, T. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 110, 563-574 (2002).
31. Hutvágner, G. & Zamore, P. D. A microRNA in a multiple-turn over RNAi enzyme complex. Science 297, 2056-2060 (2002).
32. Martinez, J. & Tuschl, T. RISC is a 5′ phosphomonoester- producing RNA endonuclease, Genes Dev. 18, 975-980 (2004).
33. Tahbaz, N. et al. Characterization of the interactions between mammalian PAZ PIWI domain proteins and Dicer. EMBO Rep. 5, 189-194 (2004).
34. Tomari, Y. et al. RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 116, 831-841 (2004).
35. Cook, H. A., Koppetsch, B. S., Wu, J. & Theurkauf, W. E. The Drosophila SDE3 homolog armitage is required for oskar mRNA silencing and embryonic axis specification. Cell 116, 817-829 (2004).
36. Khvorova, A., Reynolds, A. & Jayasena, S. D. Functional siRNAs and miRNAs exhibit strand bias. Cell 115, 209-216 (2003).
37. Schwarz, D. S. et al. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115, 199-208 (2003).
38. Carmell, M. A., Xuan, Z., Zhang, M. Q. & Hannon, G. J. The Argonaute family: tentacles that reach into RNAi, developmental control, stem-cell maintenance, and tumorigenesis. Genes Dev. 16, 2733-2742 (2002).
39. Song, J. J., Smith, S. K., Hannon, G. J. & Joshua-Tor, L. Crystal structure of Argonaute and its implications for RISC slicer activity. Science, published online 29 July 2004 (doi: 10.1126/science.1102514).
40. Ma, J. B., Ye, K. & Patel, D. J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429, 318-322 (2004).
41. Lingel, A., Simon, B., Izaurralde, E. & Sattler, M. Nucleic acid 3′-end recognition by the Argonaute2 PAZ domain. Nature Struct. Mol. Biol. 11, 576-577 (2004).
42. Elbashir, S. M., Martinez, J., Patkaniowska, A., Lendeckel, W. & Tuschl, T. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J. 20, 6877-6888 (2001).
43. Hunter, C., Sun, H. & Poethig, R. S. The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr. Biol. 13, 1734-1739 (2003).
44. Williams, R. W. & Rubin, G. M. ARGONAUTE1 is required for efficient RNA interference in Drosophila embryos. Proc. Natl Acad. Sci. USA 99, 6889-6894 (2002).
45. Sasaki, T., Shiohama, A., Minoshima, S. & Shimizu, N. Identification of eight members of the Argonaute family in the human genome. Genomics 82, 323-330 (2003).
46. Okamura, K., Ishizuka, A., Siomi, H. & Siomi, M. C. Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 18, 1655-1666 (2004).
47. Meister, G. et al. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15, 185-197 (2004).
48. Liu, J. et al. Argonaute2 is the catalytic engine of mammalian RNAi. Science, published online 29 July 2004 (doi: 10.1126/science.1102513).
49. Caudy, A. A., Myers, M., Hannon, G. J. & Hammond, S. M. Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16, 2491-2496 (2002).
50. Caudy, A. A. et al. A micrococcal nuclease homologue in RNAi effector complexes. Nature 425, 411-414 (2003).
51. Ishizuka, A., Siomi, M. C. & Siomi, H. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 16, 2497-2508 (2002).
52. Jin, P. et al. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nature Neurosci. 7, 133-117 (2004).
53. 2+-dependent endonuclease. Curr. Biol. 14, 787-791 (2004).
54. Olsen, P. H. & Ambros, V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671-680 (1999).
55. Seggerson, K., Tang, L. & Moss, E. G. Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev. Biol. 243, 215-225 (2002).
56. Kim, J. et al. Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc. Natl Acad. Sci. USA 101, 360-365 (2004).
57. Doench, J. G., Petersen, C. P. & Sharp, P. A. siRNAs can function as miRNAs. Genes Dev. 17, 438-442 (2003).
58. Saxena, S., Jonsson, Z. O. & Dutta, A. Small RNAs with imperfect match to endogenous mRNA repress translation: implications for off-target activity of siRNA in mammalian cells. J. Biol. Chem. 278, 44312-44319 (2003).
59. Wassenegger, M. & Pelissier, T. A model for RNA-mediated gene silencing in higher plants. Plant Mol. Biol. 37, 349-362 (1998).
60. Sijen, T. et al. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107, 465-476 (2001).
61. Schwarz, D.S., Hutvágner, G., Haley, B. & Zamore, P. D. Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol. Cell 10, 537-548 (2002).
62. Roignant, J. Y. et al. Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. RNA 9, 299-308 (2003).
63. Stein, P., Svoboda, P., Anger, M. & Schultz, R. M. RNAi: mammalian oocytes do it without RNA-dependent RNA polymerase. RNA 9, 187-192 (2003).
64. Waterhouse, P. M., Wang, M. & Finnegan, E. J. Role of short RNAs in gene silencing. Trends Plant Sci. 6, 297-301 (2001).
65. Gitlin, L. & Andino, R. Nucleic acid-based immune system: the antiviral potential of mammalian RNA silencing. J. Virol. 77, 7159-7165 (2003).
66. Li, W. X. & Ding, S. W. Viral suppressors of RNA silencing. Curr. Opin. Biotechnol. 12, 150-154 (2001).
67. Voinnet, O. RNA silencing as a plant immune system against viruses. Trends Genet. 17, 449-459 (2001).
68. Li, H., Li, W. X. & Ding, S. W. Induction and suppression of RNA silencing by an animal virus. Science 296, 1319-1321 (2002).
69. Vargason, J. M., Szittya, G., Burgyan, J. & Hall, T. M. Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115, 799-811 (2003).
70. Ye, K., Malinina, L. & Patel, D. J. Recognition of small interfering RNA by a viral suppressor of RNA silencing. Nature 426, 874-878 (2003).
71. Knight, S. W. & Bass, B. L. The role of RNA editing by ADARs in RNAi. Mol. Cell 10, 809-817 (2002).
72. Tonkin, L. A. & Bass, B. L. Mutations in RNAi rescue aberrant chemotaxis of ADAR mutants. Science 302, 1725 (2003).
73. Kennedy, S., Wang, D. & Ruvkun, G. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427, 645-649 (2004).
74. 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).
75. Calin, G. A. et al. Frequent deletions and down-regulation of microRNA genes miR-15 and miR-16 at 13q14 in chronic lymphocytic leukemia. Prac. Natl Acad. Sci. USA 99, 15524-15529 (2002).
76. Michael, M. Z., O'Connor, S. M., van Holst Pellekaan, N. G., Young, G. P. & James, R. J. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol. Cancer Res. 1, 882-891 (2003).
77. Moroy, T, et al. Structure and expression of hcr, a locus rearranged with c-myc in a woodchuck hepatocellular carcinoma. Oncogene 4, 59-65 (1989).
78. Gauwerky, C. E., Huebner, K., Isobe, M., Nowell, P. C. & Croce, C. M. Activation of MYC in a masked t(8;17) translocation results in an aggressive B-cell leukemia. Proc. Natl Acad. Sci. USA 86, 8867-8871 (1989).
79. Pfeffer, S. et al. Identification of virus-encoded microRNAs. Science 304, 734-736 (2004).
80. Bohmert, K. et al. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17, 170-180 (1998).
81. Verdel, A. et al. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303, 672-676 (2004).
82. Zilberman, D., Cao, X. & Jacobsen, S. E. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299, 716-719 (2003).
83. Pal-Bhadra, M., Bhadra, U. & Birchler, J. A. RNAi-related mechanism affects both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol. Cell 9, 315-327 (2002).
84. Kennerdell, J. R., Yamaguchi, S. & Carthew, R. W. RNAi is activated during Drosophila oocyte maturation in a manner dependenton aubergine and spindle-E. Genes Dev. 16, 1884-1889 (2002).
85. Tijsterman, M., Okihara, K. L., Thijssen, K. & Plasterk, R. H. PPW-1, a PAZ/PIWI protein required for efficient germline RNAi, is defective in a natural isolate of C. elegans. Curr. Biol. 12, 1535-1540 (2002).
86. Fagard, M., Boutet, S., Morel, J. B., Bellini, C. & Vaucheret, H. AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc. Natl Acad. Sci. USA 97, 11650-11654 (2000).
87. Dalmay, T., Horsefield, R., Braunstein, T. H. & Baulcombe, D. C. SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J. 20, 2069-2078 (2001).
88. Tijsterman, M., Ketting, R. F., Okihara, K. L. & Plasterk, R. H. RNA helicase MUT-14-dependent silencing triggered in C. elegans by short antisense RNAs. Science 295, 694-697 (2002).
89. Domeier, M. E. et al. A link between RNA interference and nonsense-mediated decay in Caenorhabditis elegans. Science 289, 1928-1931 (2000).
90. Mourrain, P. et al. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101, 533-542 (2000).
91. Chan, S. W. et al. RNA silencing genes control de novo DNA methylation. Science 303, 1336 (2004).
92. 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).
93. Cogoni, C. & Macino, G. Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399, 166-169 (1999).
94. Giazov, E. et al. A gene encoding an RNase D exonuclease-like protein is required for post-transcriptional silencing in Arabidopsis. Plant J. 35, 342-349 (2003).
95. 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, 133-141 (1999).
96. Winston, W. M., Molodowitch, C. & Hunter, C. P. Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295, 2456-2459 (2002).
97. Cogoni, C. & Macino, G. Posttranscriptional gene silencing in Neurospora by a RecQ DNA helicase. Science 286, 2342-2344 (1999).
98. Kidner, C. A. & Martienssen, R. A. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428, 81-84 (2004).