Transposable element dynamics and PIWI regulation impacts lncRNA and gene expression diversity in Drosophila ovarian cell cultures

Genome Research

Volumn 24, Issue 12, 2014, Pages 1977-1990

  Sytnikova, Yuliya A ^a   Rahman, Reazur ^a   Chirn, Gung Wei ^a   Clark, Josef P ^a   Lau, Nelson C ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; PIWI INTERACTING RNA; PIWI PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTOME; TRANSPOSON;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; CELL FRACTIONATION; CELL LINEAGE; CONTROLLED STUDY; DROSOPHILA; EPIGENETIC REPRESSION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC CODE; GENETIC TRANSCRIPTION; NONHUMAN; OOCYTE; OVARY CELL CULTURE; OVARY FOLLICLE CELL; RNA BINDING; RNA ISOLATION; RNA SEQUENCE; RNA SPLICING; SIGNAL TRANSDUCTION; SOMATIC CELL; TRANSPOSON; ANIMAL; BIOLOGY; CELL LINE; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING;

ANIMALS; CELL LINE; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; RNA, LONG NONCODING; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84911496009     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.178129.114     Document Type: Article

References (78)

1. Aliyari R, Wu Q, Li HW, Wang XH, Li F, Green LD, Han CS, Li WX, Ding SW. 2008. Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 4: 387-397.
2. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol 11: R106.
3. Arkhipova IR, Rodriguez F. 2013. Genetic and epigenetic changes involving (retro)transposons in animal hybrids and polyploids. Cytogenet Genome Res 140: 295-311.
4. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-W208.
5. Bowen NJ, McDonald JF. 2001. Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. Genome Res 11: 1527-1540.
6. Brasset E, Taddei AR, Arnaud F, Faye B, Fausto AM, Mazzini M, Giorgi F, Vaury C. 2006. Viral particles of the endogenous retrovirus ZAM from Drosophila melanogaster use a pre-existing endosome/exosome pathway for transfer to the oocyte. Retrovirology 3: 25.
7. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. 2007. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
8. Brown JB, Boley N, Eisman R, May GE, Stoiber MH, Duff MO, Booth BW, Wen J, Park S, Suzuki AM, et al. 2014. Diversity and dynamics of the Drosophila transcriptome. Nature 512: 393-399.
9. Cherbas L, Willingham A, Zhang D, Yang L, Zou Y, Eads BD, Carlson JW, Landolin JM, Kapranov P, Dumais J, et al. 2011. The transcriptional diversity of 25 Drosophila cell lines. Genome Res 21: 301-314.
10. Chi SW, Zang JB, Mele A, Darnell RB. 2009. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486.
11. Cho J, Chang H, Kwon SC, Kim B, Kim Y, Choe J, Ha M, Kim YK, Kim VN. 2012. LIN28A is a suppressor of ER-associated translation in embryonic stem cells. Cell 151: 765-777.
12. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, Morell M, O'Shea KS, Moran JV, Gage FH. 2009. L1 retrotransposition in human neural progenitor cells. Nature 460: 1127-1131.
13. Cowley M, Oakey RJ. 2013. Transposable elements re-wire and fine-tune the transcriptome. PLoS Genet 9: e1003234.
14. Czech B, Malone CD, Zhou R, Stark A, Schlingeheyde C, Dus M, Perrimon N, Kellis M, Wohlschlegel JA, Sachidanandam R, et al. 2008. An endogenous small interfering RNA pathway in Drosophila. Nature 453:798-802.
15. Desset S, Meignin C, Dastugue B, Vaury C. 2003. COM, a heterochromatic locus governing the control of independent endogenous retroviruses from Drosophila melanogaster. Genetics 164: 501-509.
16. Desset S, Buchon N, Meignin C, Coiffet M, Vaury C. 2008. In Drosophila melanogaster the COM locus directs the somatic silencing of two retrotransposons through both Piwi-dependent and -independent pathways. PLoS One 3: e1526.
17. Donertas D, Sienski G, Brennecke J. 2013. Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev 27: 1693-1705.
18. Ensminger AW, Yassin Y, Miron A, Isberg RR. 2012. Experimental evolution of Legionella pneumophila in mouse macrophages leads to strains with altered determinants of environmental survival. PLoS Pathog 8: e1002731.
19. Ferrari F, Plachetka A, Alekseyenko AA, Jung YL, Ozsolak F, Kharchenko PV, Park PJ, Kuroda MI. 2013. "Jump start and gain" model for dosage compensation in Drosophila based on direct sequencing of nascent transcripts. Cell Rep 5: 629-636.
20. Flynt A, Liu N, Martin R, Lai EC. 2009. Dicing of viral replication intermediates during silencing of latent Drosophila viruses. Proc Natl Acad Sci 106: 5270-5275.
21. Fontanillas P, Hartl DL, Reuter M. 2007. Genome organization and gene expression shape the transposable element distribution in the Drosophila melanogaster euchromatin. PLoS Genet 3: e210.
22. Frith MC, Saunders NF, Kobe B, Bailey TL. 2008. Discovering sequence motifs with arbitrary insertions and deletions. PLoS Comput Biol 4: e1000071.
23. Garcia-Perez JL, Morell M, Scheys JO, Kulpa DA, Morell S, Carter CC, Hammer GD, Collins KL, O'Shea KS, Menendez P, et al. 2010. Epigenetic silencing of engineered L1 retrotransposition events in human embryonic carcinoma cells. Nature 466: 769-773.
24. Ghildiyal M, Seitz H, Horwich MD, Li C, Du T, Lee S, Xu J, Kittler EL, Zapp ML, Weng Z, et al. 2008. Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells. Science 320: 1077-1081.
25. Goic B, Vodovar N, Mondotte JA, Monot C, Frangeul L, Blanc H, Gausson V, Vera-Otarola J, Cristofari G, Saleh MC. 2013. RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila. Nat Immunol 14: 396-403.
26. Haase AD, Fenoglio S, Muerdter F, Guzzardo PM, Czech B, Pappin DJ, Chen C, Gordon A, Hannon GJ. 2010. Probing the initiation and effector phases of the somatic piRNA pathway in Drosophila. Genes Dev 24: 2499-2504.
27. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M Jr, Jungkamp AC, Munschauer M, et al. 2010. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141.
28. Han JS, Boeke JD. 2004. A highly active synthetic mammalian retrotransposon. Nature 429: 314-318.
29. Huang XA, Yin H, Sweeney S, Raha D, Snyder M, Lin H. 2013. A major epigenetic programming mechanism guided by piRNAs. Dev Cell 24: 502-516.
30. Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, Patel S, Frise E, Wheeler DA, Lewis SE, Rubin GM et al. 2002. The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3: research0084.1-0084.20.
31. Kapitonov VV, Jurka J. 2008. A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet 9: 411-412.
32. Kapusta A, Kronenberg Z, Lynch VJ, Zhuo X, Ramsay L, Bourque G, Yandell M, Feschotte C. 2013. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet 9: e1003470.
33. Kawamura Y, Saito K, Kin T, Ono Y, Asai K, Sunohara T, Okada TN, Siomi MC, Siomi H. 2008. Drosophila endogenous small RNAs bind to Argonaute 2 in somatic cells. Nature 453: 793-797.
34. Kelley D, Rinn J. 2012. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol 13: R107.
35. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Res 12: 656-664.
36. Khodor YL, Rodriguez J, Abruzzi KC, Tang CH, Marr MT 2nd, Rosbash M. 2011. Nascent-seq indicates widespread cotranscriptional pre-mRNA splicing in Drosophila. Genes Dev 25: 2502-2512.
37. Khurana JS, Wang J, Xu J, Koppetsch BS, Thomson TC, Nowosielska A, Li C, Zamore PD, Weng Z, Theurkauf WE. 2011. Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 147: 1551-1563.
38. Kofler R, Betancourt AJ, Schlotterer C. 2012. Sequencing of pooled DNA samples (Pool-Seq) uncovers complex dynamics of transposable element insertions in Drosophila melanogaster. PLoS Genet 8: e1002487.
39. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
40. Lau NC. 2010. Small RNAs in the animal gonad: guarding genomes and guiding development. Int J Biochem Cell Biol 42: 1334-1347.
41. Lau NC, Robine N, Martin R, Chung WJ, Niki Y, Berezikov E, Lai EC. 2009. Abundant primary piRNAs, endo-siRNAs, and microRNAs in a Drosophila ovary cell line. Genome Res 19: 1776-1785.
42. Le Thomas A, Rogers AK, Webster A, Marinov GK, Liao SE, Perkins EM, Hur JK, Aravin AA, Toth KF. 2013. Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 27: 390-399.
43. Leung AK, Young AG, Bhutkar A, Zheng GX, Bosson AD, Nielsen CB, Sharp PA. 2011. Genome-wide identification of Ago2 binding sites from mouse embryonic stem cells with and without mature microRNAs. Nat Struct Mol Biol 18: 237-244.
44. Levin HL, Moran JV. 2011. Dynamic interactions between transposable elements and their hosts. Nat Rev Genet 12: 615-627.
45. Li C, Vagin VV, Lee S, Xu J, Ma S, Xi H, Seitz H, Horwich MD, Syrzycka M, Honda BM, et al. 2009. Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137: 509-521.
46. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map (SAM) format and SAMtools. Bioinformatics 25: 2078-2079.
47. Linheiro RS, Bergman CM. 2012. Whole genome resequencing reveals natural target site preferences of transposable elements in Drosophila melanogaster. PLoS ONE 7: e30008.
48. Mackay TF, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, Casillas S, Han Y, Magwire MM, Cridland JM, et al. 2012. The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173-178.
49. Matts JA, Sytnikova Y, Chirn GW, Igloi GL, Lau NC. 2014. Small RNA library construction from minute biological samples. Methods Mol Biol 1093: 123-136.
50. Meignin C, Dastugue B, Vaury C. 2004. Intercellular communication between germ line and somatic line is utilized to control the transcription of ZAM, an endogenous retrovirus from Drosophila melanogaster. Nucleic Acids Res 32: 3799-3806.
51. Mevel-Ninio M, Pelisson A, Kinder J, Campos AR, Bucheton A. 2007. The flamenco locus controls the gypsy and ZAM retroviruses and is required for Drosophila oogenesis. Genetics 175: 1615-1624.
52. Ng DW, Lu J, Chen ZJ. 2012. Big roles for small RNAs in polyploidy, hybrid vigor, and hybrid incompatibility. Curr Opin Plant Biol 15: 154-161.
53. Niki Y, Yamaguchi T, Mahowald AP. 2006. Establishment of stable cell lines of Drosophila germ-line stem cells. Proc Natl Acad Sci 103: 16325-16330.
54. Ohtani H, Iwasaki YW, Shibuya A, Siomi H, Siomi MC, Saito K. 2013. DmGTSF1 is necessary for Piwi-piRISC-mediated transcriptional transposon silencing in the Drosophila ovary. Genes Dev 27: 1656-1661.
55. Olivieri D, Sykora MM, Sachidanandam R, Mechtler K, Brennecke J. 2011. An in vivo RNAi assay identifies major genetic and cellular requirements for primary piRNA biogenesis in Drosophila. EMBO J 29: 3301-3317.
56. Pavesi G, Pesole G. 2006. Using Weeder for the discovery of conserved transcription factor binding sites. Curr Protoc Bioinformatics 15: 2.11.1-2.11.19.
57. Pelisson A, Song SU, Prud'homme N, Smith PA, Bucheton A, Corces VG. 1994. Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J 13: 4401-4411.
58. Pennington KL, Marr SK, Chirn GW, Marr MT II. 2013. Holo-TFIID controls the magnitude of a transcription burst and fine-tuning of transcription. Proc Natl Acad Sci 110: 7678-7683.
59. Post C, Clark JP, Sytnikova YA, Chirn GW, Lau NC. 2014. The capacity of target silencing by Drosophila PIWI and piRNAs. RNA doi: 10.1261/rna.046300.114.
60. Qi H, Watanabe T, Ku HY, Liu N, Zhong M, Lin H. 2011. The Yb body, a major site for Piwi-associated RNA biogenesis and a gateway for Piwi expression and transport to the nucleus in somatic cells. J Biol Chem 286: 3789-3797.
61. Quinlan AR, Boland MJ, Leibowitz ML, Shumilina S, Pehrson SM, Baldwin KK, Hall IM. 2011. Genome sequencing of mouse induced pluripotent stem cells reveals retroelement stability and infrequent DNA rearrangement during reprogramming. Cell Stem Cell 9: 366-373.
62. Robine N, Lau NC, Balla S, Jin Z, Okamura K, Kuramochi-Miyagawa S, Blower MD, Lai EC. 2009. A broadly conserved pathway generates 39 UTR-directed primary piRNAs. Curr Biol 19: 2066-2076.
63. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
64. Rozhkov NV, Hammell M, Hannon GJ. 2013. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev 27: 400-412.
65. Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H, Siomi MC. 2006. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20: 2214-2222.
66. Saito K, Inagaki S, Mituyama T, Kawamura Y, Ono Y, Sakota E, Kotani H, Asai K, Siomi H, Siomi MC. 2009. A regulatory circuit for piwi by the large Maf gene traffic jam in Drosophila. Nature 461: 1296-1299.
67. Saito K, Ishizu H, Komai M, Kotani H, Kawamura Y, Nishida KM, Siomi H, Siomi MC. 2010. Roles for the Yb body components Armitage and Yb in primary piRNA biogenesis in Drosophila. Genes Dev 24: 2493-2498.
68. Sarot E, Payen-Groschene G, Bucheton A, Pelisson A. 2004. Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 166: 1313-1321.
69. Sienski G, Donertas D, Brennecke J. 2012. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151: 964-980.
70. Siomi MC, Sato K, Pezic D, Aravin AA. 2011. PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246-258.
71. Spradling AC, Bellen HJ, Hoskins RA. 2011. Drosophila P elements preferentially transpose to replication origins. Proc Natl Acad Sci 108: 15948-15953.
72. Tcheressiz S, Calco V, Arnaud F, Arthaud L, Dastugue B, Vaury C. 2002. Expression of the Idefix retrotransposon in early follicle cells in the germarium of Drosophila melanogaster is determined by its LTR sequences and a specific genomic context. Mol Genet Genomics 267: 133-141.
73. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD. 2006. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313: 320-324.
74. Vourekas A, Zheng Q, Alexiou P, Maragkakis M, Kirino Y, Gregory BD, Mourelatos Z. 2012. Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis. Nat Struct Mol Biol 19: 773-781.
75. Wang L, Park HJ, Dasari S, Wang S, Kocher JP, Li W. 2013. CPAT: Coding-Potential Assessment Tool using an alignment-free logistic regression model. Nucleic Acids Res 41: e74.
76. Wu Q, Luo Y, Lu R, Lau N, Lai EC, Li WX, Ding SW. 2010. Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc Natl Acad Sci 107: 1606-1611.
77. Yin H, Lin H. 2007. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450: 304-308.
78. Zisoulis DG, Lovci MT, Wilbert ML, Hutt KR, Liang TY, Pasquinelli AE, Yeo GW. 2010. Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat Struct Mol Biol 17: 173-179.