UAP56 couples piRNA clusters to the perinuclear transposon silencing machinery

Cell

Volumn 151, Issue 4, 2012, Pages 871-884

  Zhang, Fan ^a   Wang, Jie ^a   Xu, Jia ^a   Zhang, Zhao ^a   Koppetsch, Birgit S ^a   Schultz, Nadine ^a   Vreven, Thom ^a   Meignin, Carine ^b   Davis, Ilan ^c   Zamore, Phillip D ^d,e   Weng, Zhiping ^a   Theurkauf, William E ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX PROTEIN; HETEROCHROMATIN PROTEIN 1; PIWI INTERACTING RNA; PIWI PROTEIN; PROTEIN RHINO; PROTEIN UAP56; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLUSTER ANALYSIS; FEMALE; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION;

EID: 84869016142     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.09.040     Document Type: Article

References (50)

1. A.A. Aravin, G.J. Hannon, and J. Brennecke The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race Science 318 2007 761 764 (Pubitemid 351411762)
2. J.L. Bennetzen Transposable element contributions to plant gene and genome evolution Plant Mol. Biol. 42 2000 251 269 (Pubitemid 30096120)
3. C.M. Bergman, H. Quesneville, D. Anxolabéhère, and M. Ashburner Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome Genome Biol. 7 2006 R112
4. J. Brennecke, A.A. Aravin, A. Stark, M. Dus, M. Kellis, R. Sachidanandam, and G.J. Hannon Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila Cell 128 2007 1089 1103 (Pubitemid 46427877)
5. R.J. Britten Transposable element insertions have strongly affected human evolution Proc. Natl. Acad. Sci. USA 107 2010 19945 19948
6. A.A. Caudy, M. Myers, G.J. Hannon, and S.M. Hammond Fragile X-related protein and VIG associate with the RNA interference machinery Genes Dev. 16 2002 2491 2496
7. D.F. Eberl, L.J. Lorenz, M.B. Melnick, V. Sood, P. Lasko, and N. Perrimon A new enhancer of position-effect variegation in Drosophila melanogaster encodes a putative RNA helicase that binds chromosomes and is regulated by the cell cycle Genetics 146 1997 951 963 (Pubitemid 27290979)
8. E.M. Eddy Fine structural observations on the form and distribution of nuage in germ cells of the rat Anat. Rec. 178 1974 731 757
9. E.M. Eddy Germ plasm and the differentiation of the germ cell line Int. Rev. Cytol. 43 1975 229 280
10. D. Gatfield, H. Le Hir, C. Schmitt, I.C. Braun, T. Köcher, M. Wilm, and E. Izaurralde The DExH/D box protein HEL/UAP56 is essential for mRNA nuclear export in Drosophila Curr. Biol. 11 2001 1716 1721 (Pubitemid 33037786)
11. M. Ghildiyal, and P.D. Zamore Small silencing RNAs: an expanding universe Nat. Rev. Genet. 10 2009 94 108
12. L.S. Gunawardane, K. Saito, K.M. Nishida, K. Miyoshi, Y. Kawamura, T. Nagami, H. Siomi, and M.C. Siomi A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila Science 315 2007 1587 1590 (Pubitemid 46449477)
13. A.N. Harris, and P.M. Macdonald Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C Development 128 2001 2823 2832 (Pubitemid 32701010)
14. B. Hay, L.Y. Jan, and Y.N. Jan Localization of vasa, a component of Drosophila polar granules, in maternal-effect mutants that alter embryonic anteroposterior polarity Development 109 1990 425 433 (Pubitemid 20205581)
15. D.J. Hedges, and V.P. Belancio Restless genomes humans as a model organism for understanding host-retrotransposable element dynamics Adv. Genet. 73 2011 219 262
16. M.D. Horwich, C. Li, C. Matranga, V. Vagin, G. Farley, P. Wang, and P.D. Zamore The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC Curr. Biol. 17 2007 1265 1272 (Pubitemid 47043434)
17. J.K. Jang, D.E. Sherizen, R. Bhagat, E.A. Manheim, and K.S. McKim Relationship of DNA double-strand breaks to synapsis in Drosophila J. Cell Sci. 116 2003 3069 3077 (Pubitemid 37038956)
18. O. Johnstone, and P. Lasko Interaction with eIF5B is essential for Vasa function during development Development 131 2004 4167 4178 (Pubitemid 39276187)
19. J.S. Khurana, and W. Theurkauf piRNAs, transposon silencing, and Drosophila germline development J. Cell Biol. 191 2010 905 913
20. C. Klattenhoff, and W. Theurkauf Biogenesis and germline functions of piRNAs Development 135 2008 3 9 (Pubitemid 351201476)
21. C. Klattenhoff, D.P. Bratu, N. McGinnis-Schultz, B.S. Koppetsch, H.A. Cook, and W.E. Theurkauf Drosophila rasiRNA pathway mutations disrupt embryonic axis specification through activation of an ATR/Chk2 DNA damage response Dev. Cell 12 2007 45 55 (Pubitemid 46002601)
22. C. Klattenhoff, H. Xi, C. Li, S. Lee, J. Xu, J.S. Khurana, F. Zhang, N. Schultz, B.S. Koppetsch, and A. Nowosielska The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters Cell 138 2009 1137 1149
23. P.F. Lasko, and M. Ashburner Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development Genes Dev. 4 1990 905 921
24. C. Li, V.V. Vagin, S. Lee, J. Xu, S. Ma, H. Xi, H. Seitz, M.D. Horwich, M. Syrzycka, and B.M. Honda Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies Cell 137 2009 509 521
25. L. Liang, W. Diehl-Jones, and P. Lasko Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities Development 120 1994 1201 1211 (Pubitemid 24150045)
26. A.K. Lim, and T. Kai Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster Proc. Natl. Acad. Sci. USA 104 2007 6714 6719 (Pubitemid 47175566)
27. P. Linder, and E. Jankowsky From unwinding to clamping - the DEAD box RNA helicase family Nat. Rev. Mol. Cell Biol. 12 2011 505 516
28. H. Ma, J.R. McLean, L.F. Chao, S. Mana-Capelli, M. Paramasivam, K.A. Hagstrom, K.L. Gould, and D. McCollum A highly efficient multifunctional tandem affinity purification approach applicable to diverse organisms Mol. Cell. Proteomics 11 2012 501 511
29. M. MacMorris, C. Brocker, and T. Blumenthal UAP56 levels affect viability and mRNA export in Caenorhabditis elegans RNA 9 2003 847 857 (Pubitemid 36734782)
30. J.P. Madigan, H.L. Chotkowski, and R.L. Glaser DNA double-strand break-induced phosphorylation of Drosophila histone variant H2Av helps prevent radiation-induced apoptosis Nucleic Acids Res. 30 2002 3698 3705 (Pubitemid 35012441)
31. C.D. Malone, and G.J. Hannon Small RNAs as guardians of the genome Cell 136 2009 656 668
32. C.D. Malone, J. Brennecke, M. Dus, A. Stark, W.R. McCombie, R. Sachidanandam, and G.J. Hannon Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary Cell 137 2009 522 535
33. C. Meignin, and I. Davis UAP56 RNA helicase is required for axis specification and cytoplasmic mRNA localization in Drosophila Dev. Biol. 315 2008 89 98
34. M. Mével-Ninio, A. Pelisson, J. Kinder, A.R. Campos, and A. Bucheton The flamenco locus controls the gypsy and ZAM retroviruses and is required for Drosophila oogenesis Genetics 175 2007 1615 1624 (Pubitemid 46789949)
35. D.R. Micklem, R. Dasgupta, H. Elliott, F. Gergely, C. Davidson, A. Brand, A. González-Reyes, and D. St Johnston The mago nashi gene is required for the polarisation of the oocyte and the formation of perpendicular axes in Drosophila Curr. Biol. 7 1997 468 478 (Pubitemid 27308970)
36. S.E. Mohr, S.T. Dillon, and R.E. Boswell The RNA-binding protein Tsunagi interacts with Mago Nashi to establish polarity and localize oskar mRNA during Drosophila oogenesis Genes Dev. 15 2001 2886 2899 (Pubitemid 33042058)
37. B. Montpetit, N.D. Thomsen, K.J. Helmke, M.A. Seeliger, J.M. Berger, and K. Weis A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export Nature 472 2011 238 242
38. P.A. Newmark, and R.E. Boswell The mago nashi locus encodes an essential product required for germ plasm assembly in Drosophila Development 120 1994 1303 1313 (Pubitemid 24150054)
39. P.A. Newmark, S.E. Mohr, L. Gong, and R.E. Boswell mago nashi mediates the posterior follicle cell-to-oocyte signal to organize axis formation in Drosophila Development 124 1997 3197 3207 (Pubitemid 27387096)
40. J.Q. Ni, M. Markstein, R. Binari, B. Pfeiffer, L.P. Liu, C. Villalta, M. Booker, L. Perkins, and N. Perrimon Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster Nat. Methods 5 2008 49 51
41. D. Parkhomchuk, T. Borodina, V. Amstislavskiy, M. Banaru, L. Hallen, S. Krobitsch, H. Lehrach, and A. Soldatov Transcriptome analysis by strand-specific sequencing of complementary DNA Nucleic Acids Res. 37 2009 e123
42. P. Rorth Gal4 in the Drosophila female germline Mech. Dev. 78 1998 113 118 (Pubitemid 28566217)
43. K. Saito, Y. Sakaguchi, T. Suzuki, T. Suzuki, H. Siomi, and M.C. Siomi Pimet, the Drosophila homolog of HEN1, mediates 2′-O-methylation of Piwi- interacting RNAs at their 3′ ends Genes Dev. 21 2007 1603 1608 (Pubitemid 47026364)
44. E. Sarot, G. Payen-Groschêne, A. Bucheton, and A. Pélisson Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene Genetics 166 2004 1313 1321 (Pubitemid 38507050)
45. H. Shen UAP56- a key player with surprisingly diverse roles in pre-mRNA splicing and nuclear export BMB Rep 42 2009 185 188
46. H. Shi, O. Cordin, C.M. Minder, P. Linder, and R.M. Xu Crystal structure of the human ATP-dependent splicing and export factor UAP56 Proc. Natl. Acad. Sci. USA 101 2004 17628 17633 (Pubitemid 40051937)
47. M.C. Siomi, T. Miyoshi, and H. Siomi piRNA-mediated silencing in Drosophila germlines Semin. Cell Dev. Biol. 21 2010 754 759
48. D.L. Updike, S.J. Hachey, J. Kreher, and S. Strome P granules extend the nuclear pore complex environment in the C. elegans germ line J. Cell Biol. 192 2011 939 948
49. R. Zhao, J. Shen, M.R. Green, M. MacMorris, and T. Blumenthal Crystal structure of UAP56, a DExD/H-box protein involved in pre-mRNA splicing and mRNA export Structure 12 2004 1373 1381 (Pubitemid 39092082)
50. Costes, S.V., Daelemans, D., Cho, E.H., Dobbin, Z., Pavlakis, G., and Lockett, S. (2004). Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys. J. 86, 3993-4003. (Pubitemid 38780275)