The RNase PARN-1 Trims piRNA 3′ Ends to Promote Transcriptome Surveillance in C. elegans

Cell

Volumn 164, Issue 5, 2016, Pages 974-984

  Tang, Wen ^a   Tu, Shikui ^a   Lee, Heng Chi ^a   Weng, Zhiping ^a   Mello, Craig C ^a,b  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; MESSENGER RNA; PIWI INTERACTING RNA; POLY(A) SPECIFIC RIBONUCLEASE 1; RIBONUCLEASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; ARGONAUTE PROTEIN; EXORIBONUCLEASE; POLY(A)-SPECIFIC RIBONUCLEASE; PRG-1 PROTEIN, C ELEGANS; SMALL INTERFERING RNA;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; RNA PROCESSING; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ARGONAUTE PROTEINS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; EXORIBONUCLEASES; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; MUTATION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, SMALL INTERFERING; SEQUENCE ALIGNMENT; TRANSCRIPTOME;

EID: 84959450484     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.02.008     Document Type: Article

References (83)

1. A. Ashe, A. Sapetschnig, E.M. Weick, J. Mitchell, M.P. Bagijn, A.C. Cording, A.L. Doebley, L.D. Goldstein, N.J. Lehrbach, J. Le Pen, and et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans Cell 150 2012 88 99
2. J. Aström, A. Aström, and A. Virtanen Properties of a HeLa cell 3′ exonuclease specific for degrading poly(A) tails of mammalian mRNA J. Biol. Chem. 267 1992 18154 18159
3. M.P. Bagijn, L.D. Goldstein, A. Sapetschnig, E.M. Weick, S. Bouasker, N.J. Lehrbach, M.J. Simard, and E.A. Miska Function, targets, and evolution of Caenorhabditis elegans piRNAs Science 337 2012 574 578
4. S. Barberán-Soler, L. Fontrodona, A. Ribó, A.T. Lamm, C. Iannone, J. Cerón, B. Lehner, and J. Valcárcel Co-option of the piRNA pathway for germline-specific alternative splicing of C. elegans TOR Cell Rep. 8 2014 1609 1616
5. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
6. P.J. Batista, J.G. Ruby, J.M. Claycomb, R. Chiang, N. Fahlgren, K.D. Kasschau, D.A. Chaves, W. Gu, J.J. Vasale, S. Duan, and et al. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans Mol. Cell 31 2008 67 78
7. M.J. Beanan, and S. Strome Characterization of a germ-line proliferation mutation in C. elegans Development 116 1992 755 766
8. H. Berndt, C. Harnisch, C. Rammelt, N. Stöhr, A. Zirkel, J.C. Dohm, H. Himmelbauer, J.P. Tavanez, S. Hüttelmaier, and E. Wahle Maturation of mammalian H/ACA box snoRNAs: PAPD5-dependent adenylation and PARN-dependent trimming RNA 18 2012 958 972
9. A.C. Billi, A.F. Alessi, V. Khivansara, T. Han, M. Freeberg, S. Mitani, and J.K. Kim The Caenorhabditis elegans HEN1 ortholog, HENN-1, methylates and stabilizes select subclasses of germline small RNAs PLoS Genet. 8 2012 e1002617
10. D. Brawand, M. Soumillon, A. Necsulea, P. Julien, G. Csárdi, P. Harrigan, M. Weier, A. Liechti, A. Aximu-Petri, M. Kircher, and et al. The evolution of gene expression levels in mammalian organs Nature 478 2011 343 348
11. J. Brennecke, A. Stark, R.B. Russell, and S.M. Cohen Principles of microRNA-target recognition PLoS Biol. 3 2005 e85
12. 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
13. S. Brenner The genetics of Caenorhabditis elegans Genetics 77 1974 71 94
14. M.A. Carmell, A. Girard, H.J. van de Kant, D. Bourc'his, T.H. Bestor, D.G. de Rooij, and G.J. Hannon MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline Dev. Cell 12 2007 503 514
15. G. Cecere, G.X. Zheng, A.R. Mansisidor, K.E. Klymko, and A. Grishok Promoters recognized by forkhead proteins exist for individual 21U-RNAs Mol. Cell 47 2012 734 745
16. C.C. Chen, M.J. Simard, H. Tabara, D.R. Brownell, J.A. McCollough, and C.C. Mello A member of the polymerase beta nucleotidyltransferase superfamily is required for RNA interference in C. elegans Curr. Biol. 15 2005 378 383
17. C.C. Conine, J.J. Moresco, W. Gu, M. Shirayama, D. Conte Jr., J.R. Yates 3rd, and C.C. Mello Argonautes promote male fertility and provide a paternal memory of germline gene expression in C. elegans Cell 155 2013 1532 1544
18. D. Conte Jr., L.T. MacNeil, A.J. Walhout, and C.C. Mello RNA Interference in Caenorhabditis elegans Curr. Protoc. Mol. Biol. 109 2015 1 30 30
19. P.R. Copeland, and M. Wormington The mechanism and regulation of deadenylation: identification and characterization of Xenopus PARN RNA 7 2001 875 886
20. D.N. Cox, A. Chao, J. Baker, L. Chang, D. Qiao, and H. Lin A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal Genes Dev. 12 1998 3715 3727
21. P.P. Das, M.P. Bagijn, L.D. Goldstein, J.R. Woolford, N.J. Lehrbach, A. Sapetschnig, H.R. Buhecha, M.J. Gilchrist, K.L. Howe, R. Stark, and et al. Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline Mol. Cell 31 2008 79 90
22. A. Deerberg, S. Willkomm, and T. Restle Minimal mechanistic model of siRNA-dependent target RNA slicing by recombinant human Argonaute 2 protein Proc. Natl. Acad. Sci. USA 110 2013 17850 17855
23. V.L. Feltzin, M. Khaladkar, M. Abe, M. Parisi, G.J. Hendriks, J. Kim, and N.M. Bonini The exonuclease Nibbler regulates age-associated traits and modulates piRNA length in Drosophila Aging Cell 14 2015 443 452
24. R.C. Friedman, K.K. Farh, C.B. Burge, and D.P. Bartel Most mammalian mRNAs are conserved targets of microRNAs Genome Res. 19 2009 92 105
25. C. Frøkjaer-Jensen, M.W. Davis, C.E. Hopkins, B.J. Newman, J.M. Thummel, S.P. Olesen, M. Grunnet, and E.M. Jorgensen Single-copy insertion of transgenes in Caenorhabditis elegans Nat. Genet. 40 2008 1375 1383
26. A.C. Goldstrohm, and M. Wickens Multifunctional deadenylase complexes diversify mRNA control Nat. Rev. Mol. Cell Biol. 9 2008 337 344
27. W. Gu, M. Shirayama, D. Conte Jr., J. Vasale, P.J. Batista, J.M. Claycomb, J.J. Moresco, E.M. Youngman, J. Keys, M.J. Stoltz, and et al. Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline Mol. Cell 36 2009 231 244
28. W. Gu, H.C. Lee, D. Chaves, E.M. Youngman, G.J. Pazour, D. Conte Jr., and C.C. Mello CapSeq and CIP-TAP identify Pol II start sites and reveal capped small RNAs as C. elegans piRNA precursors Cell 151 2012 1488 1500
29. B. Haley, and P.D. Zamore Kinetic analysis of the RNAi enzyme complex Nat. Struct. Mol. Biol. 11 2004 599 606
30. B.W. Han, J.H. Hung, Z. Weng, P.D. Zamore, and S.L. Ameres The 3′-to-5′ exoribonuclease Nibbler shapes the 3′ ends of microRNAs bound to Drosophila Argonaute1 Curr. Biol. 21 2011 1878 1887
31. B.W. Han, W. Wang, C. Li, Z. Weng, and P.D. Zamore Noncoding RNA. piRNA-guided transposon cleavage initiates Zucchini-dependent, phased piRNA production Science 348 2015 817 821
32. S. Honda, Y. Kirino, M. Maragkakis, P. Alexiou, A. Ohtaki, R. Murali, Z. Mourelatos, and Y. Kirino Mitochondrial protein BmPAPI modulates the length of mature piRNAs RNA 19 2013 1405 1418
33. 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
34. S. Houwing, L.M. Kamminga, E. Berezikov, D. Cronembold, A. Girard, H. van den Elst, D.V. Filippov, H. Blaser, E. Raz, C.B. Moens, and et al. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish Cell 129 2007 69 82
35. J.J. Ipsaro, A.D. Haase, S.R. Knott, L. Joshua-Tor, and G.J. Hannon The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis Nature 491 2012 279 283
36. H. Ishizu, H. Siomi, and M.C. Siomi Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines Genes Dev. 26 2012 2361 2373
37. N. Izumi, K. Shoji, Y. Sakaguchi, S. Honda, Y. Kirino, T. Suzuki, S. Katsuma, and Y. Tomari Identification and Functional Analysis of the Pre-piRNA 3′ Trimmer in Silkworms Cell 164 2016 962 973 this issue
38. L.M. Kamminga, J.C. van Wolfswinkel, M.J. Luteijn, L.J. Kaaij, M.P. Bagijn, A. Sapetschnig, E.A. Miska, E. Berezikov, and R.F. Ketting Differential impact of the HEN1 homolog HENN-1 on 21U and 26G RNAs in the germline of Caenorhabditis elegans PLoS Genet. 8 2012 e1002702
39. S. Kawaoka, N. Izumi, S. Katsuma, and Y. Tomari 3′ end formation of PIWI-interacting RNAs in vitro Mol. Cell 43 2011 1015 1022
40. I. Kawasaki, Y.H. Shim, J. Kirchner, J. Kaminker, W.B. Wood, and S. Strome PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans Cell 94 1998 635 645
41. R.F. Ketting, T.H. Haverkamp, H.G. van Luenen, and R.H. Plasterk 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
42. Y. Kirino, and Z. Mourelatos Mouse Piwi-interacting RNAs are 2′-O-methylated at their 3′ termini Nat. Struct. Mol. Biol. 14 2007 347 348
43. C. Klattenhoff, and W. Theurkauf Biogenesis and germline functions of piRNAs Development 135 2008 3 9
44. C.G. Körner, and E. Wahle Poly(A) tail shortening by a mammalian poly(A)-specific 3′-exoribonuclease J. Biol. Chem. 272 1997 10448 10456
45. C.G. Körner, M. Wormington, M. Muckenthaler, S. Schneider, E. Dehlin, and E. Wahle The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes EMBO J. 17 1998 5427 5437
46. H.C. Lee, W. Gu, M. Shirayama, E. Youngman, D. Conte Jr., and C.C. Mello C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts Cell 150 2012 78 87
47. J.E. Lee, J.Y. Lee, J. Trembly, J. Wilusz, B. Tian, and C.J. Wilusz The PARN deadenylase targets a discrete set of mRNAs for decay and regulates cell motility in mouse myoblasts PLoS Genet. 8 2012 e1002901
48. X.Z. Li, C.K. Roy, X. Dong, E. Bolcun-Filas, J. Wang, B.W. Han, J. Xu, M.J. Moore, J.C. Schimenti, Z. Weng, and P.D. Zamore An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes Mol. Cell 50 2013 67 81
49. H. Lin, and A.C. Spradling A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary Development 124 1997 2463 2476
50. L. Liu, H. Qi, J. Wang, and H. Lin PAPI, a novel TUDOR-domain protein, complexes with AGO3, ME31B and TRAL in the nuage to silence transposition Development 138 2011 1863 1873
51. N. Liu, M. Abe, L.R. Sabin, G.J. Hendriks, A.S. Naqvi, Z. Yu, S. Cherry, and N.M. Bonini The exoribonuclease Nibbler controls 3′ end processing of microRNAs in Drosophila Curr. Biol. 21 2011 1888 1893
52. M.J. Luteijn, and R.F. Ketting PIWI-interacting RNAs: from generation to transgenerational epigenetics Nat. Rev. Genet. 14 2013 523 534
53. C.D. Malone, and G.J. Hannon Small RNAs as guardians of the genome Cell 136 2009 656 668
54. 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
55. M. Marasovic, M. Zocco, and M. Halic Argonaute and Triman generate dicer-independent priRNAs and mature siRNAs to initiate heterochromatin formation Mol. Cell 52 2013 173 183
56. F. Mohn, D. Handler, and J. Brennecke Noncoding RNA. piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis Science 348 2015 812 817
57. T.A. Montgomery, Y.S. Rim, C. Zhang, R.H. Dowen, C.M. Phillips, S.E. Fischer, and G. Ruvkun PIWI associated siRNAs and piRNAs specifically require the Caenorhabditis elegans HEN1 ortholog henn-1 PLoS Genet. 8 2012 e1002616
58. H. Nishimasu, H. Ishizu, K. Saito, S. Fukuhara, M.K. Kamatani, L. Bonnefond, N. Matsumoto, T. Nishizawa, K. Nakanaga, J. Aoki, and et al. Structure and function of Zucchini endoribonuclease in piRNA biogenesis Nature 491 2012 284 287
59. M. Nousch, N. Techritz, D. Hampel, S. Millonigg, and C.R. Eckmann The Ccr4-Not deadenylase complex constitutes the main poly(A) removal activity in C. elegans J. Cell Sci. 126 2013 4274 4285
60. D. Olivieri, M.M. Sykora, R. Sachidanandam, K. Mechtler, and J. Brennecke An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila EMBO J. 29 2010 3301 3317
61. A. Pane, K. Wehr, and T. Schüpbach zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline Dev. Cell 12 2007 851 862
62. R. Petryszak, T. Burdett, B. Fiorelli, N.A. Fonseca, M. Gonzalez-Porta, E. Hastings, W. Huber, S. Jupp, M. Keays, N. Kryvych, and et al. Expression Atlas update - a database of gene and transcript expression from microarray- and sequencing-based functional genomics experiments Nucleic Acids Res. 42 2014 D926 D932
63. Y.G. Ren, L.A. Kirsebom, and A. Virtanen Coordination of divalent metal ions in the active site of poly(A)-specific ribonuclease J. Biol. Chem. 279 2004 48702 48706
64. J.G. Ruby, C. Jan, C. Player, M.J. Axtell, W. Lee, C. Nusbaum, H. Ge, and D.P. Bartel Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans Cell 127 2006 1193 1207
65. 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
66. W.E. Salomon, S.M. Jolly, M.J. Moore, P.D. Zamore, and V. Serebrov Single-Molecule Imaging Reveals that Argonaute Reshapes the Binding Properties of Its Nucleic Acid Guides Cell 162 2015 84 95
67. J.P. Saxe, M. Chen, H. Zhao, and H. Lin Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline EMBO J. 32 2013 1869 1885
68. K.A. Senti, and J. Brennecke The piRNA pathway: a fly's perspective on the guardian of the genome Trends Genet. 26 2010 499 509
69. M. Seth, M. Shirayama, W. Gu, T. Ishidate, D. Conte Jr., and C.C. Mello The C. elegans CSR-1 argonaute pathway counteracts epigenetic silencing to promote germline gene expression Dev. Cell 27 2013 656 663
70. M. Shirayama, M. Seth, H.C. Lee, W. Gu, T. Ishidate, D. Conte Jr., and C.C. Mello piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline Cell 150 2012 65 77
71. B. Simon, J.P. Kirkpatrick, S. Eckhardt, M. Reuter, E.A. Rocha, M.A. Andrade-Navarro, P. Sehr, R.S. Pillai, and T. Carlomagno Recognition of 2′-O-methylated 3′-end of piRNA by the PAZ domain of a Piwi protein Structure 19 2011 172 180
72. M. Simon, P. Sarkies, K. Ikegami, A.L. Doebley, L.D. Goldstein, J. Mitchell, A. Sakaguchi, E.A. Miska, and S. Ahmed Reduced insulin/IGF-1 signaling restores germ cell immortality to Caenorhabditis elegans Piwi mutants Cell Rep. 7 2014 762 773
73. M.C. Siomi, K. Sato, D. Pezic, and A.A. Aravin PIWI-interacting small RNAs: the vanguard of genome defence Nat. Rev. Mol. Cell Biol. 12 2011 246 258
74. H. Tabara, M. Sarkissian, W.G. Kelly, J. Fleenor, A. Grishok, L. Timmons, A. Fire, and C.C. Mello The rde-1 gene, RNA interference, and transposon silencing in C. elegans Cell 99 1999 123 132
75. Y. Tian, D.K. Simanshu, J.B. Ma, and D.J. Patel Structural basis for piRNA 2′-O-methylated 3′-end recognition by Piwi PAZ (Piwi/Argonaute/Zwille) domains Proc. Natl. Acad. Sci. USA 108 2011 903 910
76. G.W. van der Heijden, J. Castañeda, and A. Bortvin Bodies of evidence - compartmentalization of the piRNA pathway in mouse fetal prospermatogonia Curr. Opin. Cell Biol. 22 2010 752 757
77. A. Vourekas, Q. Zheng, P. Alexiou, M. Maragkakis, Y. Kirino, B.D. Gregory, and Z. Mourelatos Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis Nat. Struct. Mol. Biol. 19 2012 773 781
78. G. Wang, and V. Reinke A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis Curr. Biol. 18 2008 861 867
79. C.J. Wedeles, M.Z. Wu, and J.M. Claycomb Protection of germline gene expression by the C. elegans Argonaute CSR-1 Dev. Cell 27 2013 664 671
80. E.M. Weick, and E.A. Miska piRNAs: from biogenesis to function Development 141 2014 3458 3471
81. E.M. Weick, P. Sarkies, N. Silva, R.A. Chen, S.M. Moss, A.C. Cording, J. Ahringer, E. Martinez-Perez, and E.A. Miska PRDE-1 is a nuclear factor essential for the biogenesis of Ruby motif-dependent piRNAs in C. elegans Genes Dev. 28 2014 783 796
82. M. Yoda, D. Cifuentes, N. Izumi, Y. Sakaguchi, T. Suzuki, A.J. Giraldez, and Y. Tomari Poly(A)-specific ribonuclease mediates 3′-end trimming of Argonaute2-cleaved precursor microRNAs Cell Rep. 5 2013 715 726
83. Y. Zuo, and M.P. Deutscher Exoribonuclease superfamilies: structural analysis and phylogenetic distribution Nucleic Acids Res. 29 2001 1017 1026