Small RNA in the nucleus: The RNA-chromatin ping-pong

Current Opinion in Genetics and Development

Volumn 22, Issue 2, 2012, Pages 164-171

  Olovnikov, Ivan ^a,b   Aravin, Alexei A ^a   Fejes Toth, Katalin ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; DICER; HISTONE H3; MESSENGER RNA; PIWI INTERACTING RNA; SMALL INTERFERING RNA;

CELL NUCLEUS; CENTROMERE; CHROMATIN; CHROMATIN STRUCTURE; COMPLEX FORMATION; DNA METHYLATION; DROSOPHILA; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; GENOME; GERM CELL; HISTONE METHYLATION; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SCHIZOSACCHAROMYCES POMBE; TRANSPOSON;

ANIMALS; CELL NUCLEUS; CHROMATIN; GENE EXPRESSION REGULATION; HUMANS; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC;

ANIMALIA; EUKARYOTA; SCHIZOSACCHAROMYCETACEAE;

EID: 84860369511     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2012.01.002     Document Type: Review

References (68)

1. Filion G.J., van Bemmel J.G., Braunschweig U., Talhout W., Kind J., Ward L.D., Brugman W., de Castro I.J., Kerkhoven R.M., Bussemaker H.J., et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 2010, 143:212-224.
2. Dorsett D. Cohesin: genomic insights into controlling gene transcription and development. Current Opinion in Genetics & Development 2011, 21:199-206.
3. Millau J.F., Gaudreau L. CTCF, cohesin, and histone variants: connecting the genome. Biochemistry and Cell Biology = Biochimie et biologie cellulaire 2011, 89:505-513.
4. Kohler C., Villar C.B. Programming of gene expression by Polycomb group proteins. Trends in Cell Biology 2008, 18:236-243.
5. Sugiyama T., Cam H.P., Sugiyama R., Noma K., Zofall M., Kobayashi R., Grewal S.I. SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 2007, 128:491-504.
6. Pirrotta V., Li H.-B. A view of nuclear Polycomb bodies. Current Opinion in Genetics & Development 2012, 22:101-109.
7. Gupta R.A., Shah N., Wang K.C., Kim J., Horlings H.M., Wong D.J., Tsai M.C., Hung T., Argani P., Rinn J.L., et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010, 464:1071-1076.
8. Guttman M., Donaghey J., Carey B.W., Garber M., Grenier J.K., Munson G., Young G., Lucas A.B., Ach R., Bruhn L., et al. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011, 477:295-300.
9. Wutz A. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nature Reviews. Genetics 2011, 12:542-553.
10. Flynn R.A., Chang H.Y. Active chromatin and noncoding RNAs: an intimate relationship. Current Opinion in Genetics & Development 2012, 22:172-178.
11. Chu C., Qu K., Zhong F.L., Artandi S.E., Chang H.Y. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Molecular Cell 2011, 44:667-678.
12. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
13. Meister G., Tuschl T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431:343-349.
14. Lee R.C., Ambros V. An extensive class of small RNAs in Caenorhabditis elegans. Science 2001, 294:862-864.
15. Lau N.C., Lim L.P., Weinstein E.G., Bartel D.P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001, 294:858-862.
16. Lagos-Quintana M., Rauhut R., Lendeckel W., Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001, 294:853-858.
17. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
18. Grewal S.I. RNAi-dependent formation of heterochromatin and its diverse functions. Current Opinion in Genetics & Development 2010, 20:134-141.
19. Mochizuki K. RNA-directed epigenetic regulation of DNA rearrangements. Essays in Biochemistry 2010, 48:89-100.
20. Matzke M., Kanno T., Daxinger L., Huettel B., Matzke A.J. RNA-mediated chromatin-based silencing in plants. Current Opinion in Cell Biology 2009, 21:367-376.
21. Huff J.T., Zilberman D. Regulation of biological accuracy, precision, and memory by plant chromatin organization. Current Opinion in Genetics & Development 2012, 22:132-138.
22. Reyes-Turcu F.E., Grewal S.I.S. Different means, same end-heterochromatin formation by RNAi and RNAi-independent RNA processing factors in fission yeast. Current Opinion in Genetics & Development 2012, 22:156-163.
23. 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 2002, 297:1833-1837.
24. Mochizuki K., Fine N.A., Fujisawa T., Gorovsky M.A. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell 2002, 110:689-699.
25. Dalmay T., Hamilton A., Mueller E., Baulcombe D.C. Potato virus X amplicons in arabidopsis mediate genetic and epigenetic gene silencing. The Plant Cell 2000, 12:369-379.
26. Sugiyama T., Cam H., Verdel A., Moazed D., Grewal S.I. RNA-dependent RNA polymerase is an essential component of a self-enforcing loop coupling heterochromatin assembly to siRNA production. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:152-157.
27. 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 2004, 303:672-676.
28. Noma K., Sugiyama T., Cam H., Verdel A., Zofall M., Jia S., Moazed D., Grewal S.I. RITS acts in cis to promote RNA interference-mediated transcriptional and post-transcriptional silencing. Nature Genetics 2004, 36:1174-1180.
29. Motamedi M.R., Verdel A., Colmenares S.U., Gerber S.A., Gygi S.P., Moazed D. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 2004, 119:789-802.
30. Zhang X., Yazaki J., Sundaresan A., Cokus S., Chan S.W., Chen H., Henderson I.R., Shinn P., Pellegrini M., Jacobsen S.E., et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 2006, 126:1189-1201.
31. Herr A.J., Jensen M.B., Dalmay T., Baulcombe D.C. RNA polymerase IV directs silencing of endogenous DNA. Science 2005, 308:118-120.
32. Zhang X., Henderson I.R., Lu C., Green P.J., Jacobsen S.E. Role of RNA polymerase IV in plant small RNA metabolism. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:4536-4541.
33. Kanno T., Huettel B., Mette M.F., Aufsatz W., Jaligot E., Daxinger L., Kreil D.P., Matzke M., Matzke A.J. Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nature Genetics 2005, 37:761-765.
34. Mosher R.A., Schwach F., Studholme D., Baulcombe D.C. PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:3145-3150.
35. Pontier D., Yahubyan G., Vega D., Bulski A., Saez-Vasquez J., Hakimi M.A., Lerbs-Mache S., Colot V., Lagrange T. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes & Development 2005, 19:2030-2040.
36. Weinmann L., Hock J., Ivacevic T., Ohrt T., Mutze J., Schwille P., Kremmer E., Benes V., Urlaub H., Meister G. Importin 8 is a gene silencing factor that targets argonaute proteins to distinct mRNAs. Cell 2009, 136:496-507.
37. Morris K.V., Chan S.W., Jacobsen S.E., Looney D.J. Small interfering RNA-induced transcriptional gene silencing in human cells. Science 2004, 305:1289-1292.
38. Claycomb J.M., Batista P.J., Pang K.M., Gu W., Vasale J.J., van Wolfswinkel J.C., Chaves D.A., Shirayama M., Mitani S., Ketting R.F., et al. The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 2009, 139:123-134.
39. Vagin V.V., Sigova A., Li C., Seitz H., Gvozdev V., Zamore P.D. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006, 313:320-324.
40. Siomi M.C., Sato K., Pezic D., Aravin A.A. PIWI-interacting small RNAs: the vanguard of genome defence. Nature Reviews. Molecular Cell Biology 2011, 12:246-258.
41. Senti K.A., Brennecke J. The piRNA pathway: a fly's perspective on the guardian of the genome. Trends in Genetics: TIG 2010, 26:499-509.
42. Khurana J.S., Theurkauf W. piRNAs, transposon silencing, and Drosophila germline development. The Journal of Cell Biology 2010, 191:905-913.
43. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
44. Moshkovich N., Lei E.P. HP1 recruitment in the absence of argonaute proteins in Drosophila. PLoS Genetics 2010, 6:e1000880.
45. Rangan P., Malone C.D., Navarro C., Newbold S.P., Hayes P.S., Sachidanandam R., Hannon G.J., Lehmann R. piRNA production requires heterochromatin formation in Drosophila. Current Biology: CB 2011, 21:1373-1379.
46. Josse T., Teysset L., Todeschini A.L., Sidor C.M., Anxolabehere D., Ronsseray S. Telomeric trans-silencing: an epigenetic repression combining RNA silencing and heterochromatin formation. PLoS Genetics 2007, 3:1633-1643.
47. Todeschini A.L., Teysset L., Delmarre V., Ronsseray S. The epigenetic trans-silencing effect in Drosophila involves maternally-transmitted small RNAs whose production depends on the piRNA pathway and HP1. PloS One 2010, 5:e11032.
48. Muerdter F., Olovnikov I., Molaro A., Rozhkov N., Czech B., Gordon A., Hannon G.J., Aravin A.A. Production of artificial piRNAs in flies and mice. RNA 2012, 18:42-52.
49. Marin L., Lehmann M., Nouaud D., Izaabel H., Anxolabehere D., Ronsseray S. P-Element repression in Drosophila melanogaster by a naturally occurring defective telomeric P copy. Genetics 2000, 155:1841-1854.
50. Klattenhoff C., Xi H., Li C., Lee S., Xu J., Khurana J.S., Zhang F., Schultz N., Koppetsch B.S., Nowosielska A., et al. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 2009, 138:1137-1149.
51. Pane A., Jiang P., Zhao D.Y., Singh M., Schupbach T. The Cutoff protein regulates piRNA cluster expression and piRNA production in the Drosophila germline. The EMBO Journal 2011, 30:4601-4615.
52. Aravin A.A., Sachidanandam R., Bourc'his D., Schaefer C., Pezic D., Toth K.F., Bestor T., Hannon G.J. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Molecular Cell 2008, 31:785-799.
53. Cox D.N., Chao A., Lin H. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 2000, 127:503-514.
54. Carmell M.A., Girard A., van de Kant H.J., Bourc'his D., Bestor T.H., de Rooij D.G., Hannon G.J. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Developmental Cell 2007, 12:503-514.
55. Kuramochi-Miyagawa S., Watanabe T., Gotoh K., Totoki Y., Toyoda A., Ikawa M., Asada N., Kojima K., Yamaguchi Y., Ijiri T.W., et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes & Development 2008, 22:908-917.
56. Bourc'his D., Bestor T.H. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004, 431:96-99.
57. Watanabe T., Tomizawa S., Mitsuya K., Totoki Y., Yamamoto Y., Kuramochi-Miyagawa S., Iida N., Hoki Y., Murphy P.J., Toyoda A., et al. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 2011, 332:848-852.
58. Aravin A.A., Bourc'his D. Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes & Development 2008, 22:970-975.
59. Saito K., Inagaki S., Mituyama T., Kawamura Y., Ono Y., Sakota E., Kotani H., Asai K., Siomi H., Siomi M.C. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 2009, 461:1296-1299.
60. Grimaud C., Bantignies F., Pal-Bhadra M., Ghana P., Bhadra U., Cavalli G. RNAi components are required for nuclear clustering of Polycomb group response elements. Cell 2006, 124:957-971.
61. Yin H., Lin H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 2007, 450:304-308.
62. 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 2004, 303:669-672.
63. Brower-Toland B., Findley S.D., Jiang L., Liu L., Yin H., Dus M., Zhou P., Elgin S.C., Lin H. Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes & Development 2007, 21:2300-2311.
64. Shpiz S., Olovnikov I., Sergeeva A., Lavrov S., Abramov Y., Savitsky M., Kalmykova A. Mechanism of the piRNA-mediated silencing of Drosophila telomeric retrotransposons. Nucleic Acids Research 2011.
65. Shpiz S., Kwon D., Rozovsky Y., Kalmykova A. rasiRNA pathway controls antisense expression of Drosophila telomeric retrotransposons in the nucleus. Nucleic Acids Research 2009, 37:268-278.
66. Chambeyron S., Popkova A., Payen-Groschene G., Brun C., Laouini D., Pelisson A., Bucheton A. piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:14964-14969.
67. Klenov M.S., Lavrov S.A., Stolyarenko A.D., Ryazansky S.S., Aravin A.A., Tuschl T., Gvozdev V.A. Repeat-associated siRNAs cause chromatin silencing of retrotransposons in the Drosophila melanogaster germline. Nucleic Acids Research 2007, 35:5430-5438.
68. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.