Cutoff Suppresses RNA Polymerase II Termination to Ensure Expression of piRNA Precursors

Molecular Cell

Volumn 63, Issue 1, 2016, Pages 97-109

  Chen, Yung Chia Ariel ^a   Stuwe, Evelyn ^a,b   Luo, Yicheng ^a   Ninova, Maria ^a   Le Thomas, Adrien ^a   Rozhavskaya, Ekaterina ^a   Li, Sisi ^c   Vempati, Sivani ^a   Laver, John D ^d   Patel, Dinshaw J ^c   Smibert, Craig A ^d   Lipshitz, Howard D ^d   Fejes Toth, Katalin ^a   Aravin, Alexei A ^a  

^a California Institute of Technology   (United States)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; EXONUCLEASE; EXONUCLEASE RAT1; PIWI INTERACTING RNA; POLYADENYLATED RNA; RNA HELICASE; RNA POLYMERASE II; RNA PRECURSOR; UNCLASSIFIED DRUG; ADENOSINE; CHROMATIN; CUTOFF PROTEIN, DROSOPHILA; DEADLOCK PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; EXORIBONUCLEASE; MICROTUBULE ASSOCIATED PROTEIN; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN; POLYADENOSINE; POLYMER; PROTEIN BINDING; RHINO PROTEIN, DROSOPHILA; RNA BINDING PROTEIN; SMALL INTERFERING RNA;

ARTICLE; CHROMATIN; COMPARATIVE STUDY; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION; GENE FUNCTION; NONHUMAN; PROTEIN DEPLETION; REPORTER GENE; RHINO DEADLOCK AND CUTOFF COMPLEX; RNA CLEAVAGE; RNA DEGRADATION; RNA INTERFERENCE; RNA SEQUENCE; RNA TRANSCRIPTION; TRANSCRIPTION TERMINATION; ANIMAL; BINDING SITE; BIOLOGY; BIOSYNTHESIS; DROSOPHILA MELANOGASTER; ENZYMOLOGY; GENETIC DATABASE; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; RNA STABILITY; TRANSGENIC ANIMAL;

ADENOSINE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BINDING SITES; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EXORIBONUCLEASES; GENES, REPORTER; MICROTUBULE-ASSOCIATED PROTEINS; MULTIPROTEIN COMPLEXES; POLYMERS; PROTEIN BINDING; RNA POLYMERASE II; RNA STABILITY; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; TRANSCRIPTION TERMINATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84992316144     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.05.010     Document Type: Article

References (32)

1. Aravin, A.A., Hannon, G.J., Brennecke, J., The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318 (2007), 761–764.
2. 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 128 (2007), 1089–1103.
3. Chang, J.H., Jiao, X., Chiba, K., Oh, C., Martin, C.E., Kiledjian, M., Tong, L., Dxo1 is a new type of eukaryotic enzyme with both decapping and 5′-3′ exoribonuclease activity. Nat. Struct. Mol. Biol. 19 (2012), 1011–1017.
4. Chen, Y., Pane, A., Schüpbach, T., Cutoff and aubergine mutations result in retrotransposon upregulation and checkpoint activation in Drosophila. Curr. Biol. 17 (2007), 637–642.
5. Czech, B., Preall, J.B., McGinn, J., Hannon, G.J., A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol. Cell 50 (2013), 749–761.
6. de Vanssay, A., Bougé, A.L., Boivin, A., Hermant, C., Teysset, L., Delmarre, V., Antoniewski, C., Ronsseray, S., Paramutation in Drosophila linked to emergence of a piRNA-producing locus. Nature 490 (2012), 112–115.
7. Gonatopoulos-Pournatzis, T., Cowling, V.H., Cap-binding complex (CBC). Biochem. J. 457 (2014), 231–242.
8. Goriaux, C., Desset, S., Renaud, Y., Vaury, C., Brasset, E., Transcriptional properties and splicing of the flamenco piRNA cluster. EMBO Rep. 15 (2014), 411–418.
9. Hur, J.K., Luo, Y., Moon, S., Ninova, M., Marinov, G.K., Chung, Y.D., Aravin, A.A., Splicing-independent loading of TREX on nascent RNA is required for efficient expression of dual-strand piRNA clusters in Drosophila. Genes Dev. 30 (2016), 840–855.
10. Jiao, X., Chang, J.H., Kilic, T., Tong, L., Kiledjian, M., A mammalian pre-mRNA 5′ end capping quality control mechanism and an unexpected link of capping to pre-mRNA processing. Mol. Cell 50 (2013), 104–115.
11. Keryer-Bibens, C., Barreau, C., Osborne, H.B., Tethering of proteins to RNAs by bacteriophage proteins. Biol. Cell 100 (2008), 125–138.
12. Khodor, Y.L., Rodriguez, J., Abruzzi, K.C., Tang, C.H., Marr, M.T. 2nd, Rosbash, M., Nascent-seq indicates widespread cotranscriptional pre-mRNA splicing in Drosophila. Genes Dev. 25 (2011), 2502–2512.
13. Khurana, J.S., Wang, J., Xu, J., Koppetsch, B.S., Thomson, T.C., Nowosielska, A., Li, C., Zamore, P.D., Weng, Z., Theurkauf, W.E., Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 147 (2011), 1551–1563.
14. Kim, M., Krogan, N.J., Vasiljeva, L., Rando, O.J., Nedea, E., Greenblatt, J.F., Buratowski, S., The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II. Nature 432 (2004), 517–522.
15. 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 138 (2009), 1137–1149.
16. Le Thomas, A., Stuwe, E., Li, S., Du, J., Marinov, G., Rozhkov, N., Chen, Y.C., Luo, Y., Sachidanandam, R., Toth, K.F., et al. Transgenerationally inherited piRNAs trigger piRNA biogenesis by changing the chromatin of piRNA clusters and inducing precursor processing. Genes Dev. 28 (2014), 1667–1680.
17. Malone, C.D., Hannon, G.J., Small RNAs as guardians of the genome. Cell 136 (2009), 656–668.
18. Mohn, F., Sienski, G., Handler, D., Brennecke, J., The rhino-deadlock-cutoff complex licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila. Cell 157 (2014), 1364–1379.
19. Muerdter, F., Olovnikov, I., Molaro, A., Rozhkov, N.V., Czech, B., Gordon, A., Hannon, G.J., Aravin, A.A., Production of artificial piRNAs in flies and mice. RNA 18 (2012), 42–52.
20. Nudler, E., Gottesman, M.E., Transcription termination and anti-termination in E. coli. Genes Cells 7 (2002), 755–768.
21. Pane, A., Jiang, P., Zhao, D.Y., Singh, M., Schüpbach, T., The Cutoff protein regulates piRNA cluster expression and piRNA production in the Drosophila germline. EMBO J. 30 (2011), 4601–4615.
22. Proudfoot, N.J., Ending the message: poly(A) signals then and now. Genes Dev. 25 (2011), 1770–1782.
23. 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 Res. 39 (2011), 8703–8711.
24. Siomi, M.C., Sato, K., Pezic, D., Aravin, A.A., PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 12 (2011), 246–258.
25. 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, 5, 2010, e11032.
26. Venken, K.J., Schulze, K.L., Haelterman, N.A., Pan, H., He, Y., Evans-Holm, M., Carlson, J.W., Levis, R.W., Spradling, A.C., Hoskins, R.A., Bellen, H.J., MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nat. Methods 8 (2011), 737–743.
27. West, S., Gromak, N., Proudfoot, N.J., Human 5′—> 3′ exonuclease Xrn2 promotes transcription termination at co-transcriptional cleavage sites. Nature 432 (2004), 522–525.
28. Xiang, S., Cooper-Morgan, A., Jiao, X., Kiledjian, M., Manley, J.L., Tong, L., Structure and function of the 5′—>3′ exoribonuclease Rat1 and its activating partner Rai1. Nature 458 (2009), 784–788.
29. Xue, Y., Bai, X., Lee, I., Kallstrom, G., Ho, J., Brown, J., Stevens, A., Johnson, A.W., Saccharomyces cerevisiae RAI1 (YGL246c) is homologous to human DOM3Z and encodes a protein that binds the nuclear exoribonuclease Rat1p. Mol. Cell. Biol. 20 (2000), 4006–4015.
30. Yu, B., Cassani, M., Wang, M., Liu, M., Ma, J., Li, G., Zhang, Z., Huang, Y., Structural insights into Rhino-mediated germline piRNA cluster formation. Cell Res. 25 (2015), 525–528.
31. Zhang, F., Wang, J., Xu, J., Zhang, Z., Koppetsch, B.S., Schultz, N., Vreven, T., Meignin, C., Davis, I., Zamore, P.D., et al. UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery. Cell 151 (2012), 871–884.
32. Zhang, Z., Wang, J., Schultz, N., Zhang, F., Parhad, S.S., Tu, S., Vreven, T., Zamore, P.D., Weng, Z., Theurkauf, W.E., The HP1 homolog rhino anchors a nuclear complex that suppresses piRNA precursor splicing. Cell 157 (2014), 1353–1363.