2,435
Views
46
CrossRef citations to date
0
Altmetric
Review

Noisy silence

Non-coding RNA and heterochromatin formation at repetitive elements

, &
Pages 53-61 | Received 07 Aug 2013, Accepted 13 Sep 2013, Published online: 11 Oct 2013

References

  • Lee JT. Epigenetic regulation by long noncoding RNAs. Science 2012; 338:1435 - 9; http://dx.doi.org/10.1126/science.1231776; PMID: 23239728
  • Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell 2011; 43:904 - 14; http://dx.doi.org/10.1016/j.molcel.2011.08.018; PMID: 21925379
  • Sleutels F, Zwart R, Barlow DP. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 2002; 415:810 - 3; http://dx.doi.org/10.1038/415810a; PMID: 11845212
  • Mancini-DiNardo D, Steele SJ, Levorse JM, Ingram RS, Tilghman SM. Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev 2006; 20:1268 - 82; http://dx.doi.org/10.1101/gad.1416906; PMID: 16702402
  • Williamson CM, Ball ST, Dawson C, Mehta S, Beechey CV, Fray M, Teboul L, Dear TN, Kelsey G, Peters J. Uncoupling antisense-mediated silencing and DNA methylation in the imprinted Gnas cluster. PLoS Genet 2011; 7:e1001347; http://dx.doi.org/10.1371/journal.pgen.1001347; PMID: 21455290
  • Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007; 129:1311 - 23; http://dx.doi.org/10.1016/j.cell.2007.05.022; PMID: 17604720
  • Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010; 464:1071 - 6; http://dx.doi.org/10.1038/nature08975; PMID: 20393566
  • Maamar H, Cabili MN, Rinn J, Raj A. linc-HOXA1 is a noncoding RNA that represses Hoxa1 transcription in cis. Genes Dev 2013; 27:1260 - 71; http://dx.doi.org/10.1101/gad.217018.113; PMID: 23723417
  • Klattenhoff CA, Scheuermann JC, Surface LE, Bradley RK, Fields PA, Steinhauser ML, Ding H, Butty VL, Torrey L, Haas S, et al. Braveheart, a long noncoding RNA required for cardiovascular lineage commitment. Cell 2013; 152:570 - 83; http://dx.doi.org/10.1016/j.cell.2013.01.003; PMID: 23352431
  • Feng J, Bi C, Clark BS, Mady R, Shah P, Kohtz JD. The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev 2006; 20:1470 - 84; http://dx.doi.org/10.1101/gad.1416106; PMID: 16705037
  • Lanz RB, McKenna NJ, Onate SA, Albrecht U, Wong J, Tsai SY, Tsai MJ, O’Malley BW. A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 1999; 97:17 - 27; http://dx.doi.org/10.1016/S0092-8674(00)80711-4; PMID: 10199399
  • Shamovsky I, Ivannikov M, Kandel ES, Gershon D, Nudler E. RNA-mediated response to heat shock in mammalian cells. Nature 2006; 440:556 - 60; http://dx.doi.org/10.1038/nature04518; PMID: 16554823
  • Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet 2009; 10:155 - 9; http://dx.doi.org/10.1038/nrg2521; PMID: 19188922
  • Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 2009; 23:1494 - 504; http://dx.doi.org/10.1101/gad.1800909; PMID: 19571179
  • Malecová B, Morris KV. Transcriptional gene silencing through epigenetic changes mediated by non-coding RNAs. Curr Opin Mol Ther 2010; 12:214 - 22; PMID: 20373265
  • Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem 2012; 81:145 - 66; http://dx.doi.org/10.1146/annurev-biochem-051410-092902; PMID: 22663078
  • Bühler M, Moazed D. Transcription and RNAi in heterochromatic gene silencing. Nat Struct Mol Biol 2007; 14:1041 - 8; http://dx.doi.org/10.1038/nsmb1315; PMID: 17984966
  • Azzalin CM, Lingner J. Telomeres: the silence is broken. Cell Cycle 2008; 7:1161 - 5; http://dx.doi.org/10.4161/cc.7.9.5836; PMID: 18418035
  • Schoeftner S, Blasco MAA. A ‘higher order’ of telomere regulation: telomere heterochromatin and telomeric RNAs. EMBO J 2009; 28:2323 - 36; http://dx.doi.org/10.1038/emboj.2009.197; PMID: 19629032
  • Ahmad K, Henikoff S. Modulation of a transcription factor counteracts heterochromatic gene silencing in Drosophila. Cell 2001; 104:839 - 47; http://dx.doi.org/10.1016/S0092-8674(01)00281-1; PMID: 11290322
  • Zofall M, Grewal SI. Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol Cell 2006; 22:681 - 92; http://dx.doi.org/10.1016/j.molcel.2006.05.010; PMID: 16762840
  • Chen ES, Zhang K, Nicolas E, Cam HP, Zofall M, Grewal SI. Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 2008; 451:734 - 7; http://dx.doi.org/10.1038/nature06561; PMID: 18216783
  • Santoro R, Li J, Grummt I. The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat Genet 2002; 32:393 - 6; http://dx.doi.org/10.1038/ng1010; PMID: 12368916
  • Xie W, Ling T, Zhou Y, Feng W, Zhu Q, Stunnenberg HG, Grummt I, Tao W. The chromatin remodeling complex NuRD establishes the poised state of rRNA genes characterized by bivalent histone modifications and altered nucleosome positions. Proc Natl Acad Sci U S A 2012; 109:8161 - 6; http://dx.doi.org/10.1073/pnas.1201262109; PMID: 22570494
  • Li J, Längst G, Grummt I. NoRC-dependent nucleosome positioning silences rRNA genes. EMBO J 2006; 25:5735 - 41; http://dx.doi.org/10.1038/sj.emboj.7601454; PMID: 17139253
  • Strohner R, Nemeth A, Jansa P, Hofmann-Rohrer U, Santoro R, Längst G, Grummt I. NoRC--a novel member of mammalian ISWI-containing chromatin remodeling machines. EMBO J 2001; 20:4892 - 900; http://dx.doi.org/10.1093/emboj/20.17.4892; PMID: 11532953
  • Zhou Y, Santoro R, Grummt I. The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J 2002; 21:4632 - 40; http://dx.doi.org/10.1093/emboj/cdf460; PMID: 12198165
  • Mayer C, Schmitz KM, Li J, Grummt I, Santoro R. Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 2006; 22:351 - 61; http://dx.doi.org/10.1016/j.molcel.2006.03.028; PMID: 16678107
  • Guetg C, Santoro R. Noncoding RNAs link PARP1 to heterochromatin. Cell Cycle 2012; 11:2217 - 8; http://dx.doi.org/10.4161/cc.20622; PMID: 22617384
  • Moss T, Boseley PG, Birnstiel ML. More ribosomal spacer sequences from Xenopus laevis. Nucleic Acids Res 1980; 8:467 - 85; http://dx.doi.org/10.1093/nar/8.3.467; PMID: 7003549
  • Cassidy BG, Yang-Yen HF, Rothblum LI. Additional RNA polymerase I initiation site within the nontranscribed spacer region of the rat rRNA gene. Mol Cell Biol 1987; 7:2388 - 96; PMID: 3614195
  • Kuhn A, Grummt I. A novel promoter in the mouse rDNA spacer is active in vivo and in vitro. EMBO J 1987; 6:3487 - 92; PMID: 3428263
  • Mayer C, Neubert M, Grummt I. The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep 2008; 9:774 - 80; http://dx.doi.org/10.1038/embor.2008.109; PMID: 18600236
  • Santoro R, Schmitz KM, Sandoval J, Grummt I. Intergenic transcripts originating from a subclass of ribosomal DNA repeats silence ribosomal RNA genes in trans. EMBO Rep 2010; 11:52 - 8; http://dx.doi.org/10.1038/embor.2009.254; PMID: 20010804
  • Schmitz KM, Mayer C, Postepska A, Grummt I. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev 2010; 24:2264 - 9; http://dx.doi.org/10.1101/gad.590910; PMID: 20952535
  • Santoro R, Grummt I. Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol Cell 2001; 8:719 - 25; http://dx.doi.org/10.1016/S1097-2765(01)00317-3; PMID: 11583633
  • Bierhoff H, Schmitz K, Maass F, Ye J, Grummt I. Noncoding transcripts in sense and antisense orientation regulate the epigenetic state of ribosomal RNA genes. Cold Spring Harb Symp Quant Biol 2010; 75:357 - 64; http://dx.doi.org/10.1101/sqb.2010.75.060; PMID: 21502405
  • Killen MW, Stults DM, Adachi N, Hanakahi L, Pierce AJ. Loss of Bloom syndrome protein destabilizes human gene cluster architecture. Hum Mol Genet 2009; 18:3417 - 28; http://dx.doi.org/10.1093/hmg/ddp282; PMID: 19542097
  • Stults DM, Killen MW, Williamson EP, Hourigan JS, Vargas HD, Arnold SM, Moscow JA, Pierce AJ. Human rRNA gene clusters are recombinational hotspots in cancer. Cancer Res 2009; 69:9096 - 104; http://dx.doi.org/10.1158/0008-5472.CAN-09-2680; PMID: 19920195
  • Henikoff S, Ahmad K, Malik HS. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 2001; 293:1098 - 102; http://dx.doi.org/10.1126/science.1062939; PMID: 11498581
  • Schueler MG, Sullivan BA. Structural and functional dynamics of human centromeric chromatin. Annu Rev Genomics Hum Genet 2006; 7:301 - 13; http://dx.doi.org/10.1146/annurev.genom.7.080505.115613; PMID: 16756479
  • Buscaino A, Allshire R, Pidoux A. Building centromeres: home sweet home or a nomadic existence?. Curr Opin Genet Dev 2010; 20:118 - 26; http://dx.doi.org/10.1016/j.gde.2010.01.006; PMID: 20206496
  • Hayden KE. Human centromere genomics: now it’s personal. Chromosome Res 2012; 20:621 - 33; http://dx.doi.org/10.1007/s10577-012-9295-y; PMID: 22801774
  • Black BE, Bassett EA. The histone variant CENP-A and centromere specification. Curr Opin Cell Biol 2008; 20:91 - 100; http://dx.doi.org/10.1016/j.ceb.2007.11.007; PMID: 18226513
  • Perpelescu M, Fukagawa T. The ABCs of CENPs. Chromosoma 2011; 120:425 - 46; http://dx.doi.org/10.1007/s00412-011-0330-0; PMID: 21751032
  • Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 2004; 18:1251 - 62; http://dx.doi.org/10.1101/gad.300704; PMID: 15145825
  • Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, Northrop EL, Hannan R, Saffery R, Shaw ML, Williams E, et al. Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res 2007; 17:1146 - 60; http://dx.doi.org/10.1101/gr.6022807; PMID: 17623812
  • Németh A, Conesa A, Santoyo-Lopez J, Medina I, Montaner D, Péterfia B, Solovei I, Cremer T, Dopazo J, Längst G. Initial genomics of the human nucleolus. PLoS Genet 2010; 6:e1000889; http://dx.doi.org/10.1371/journal.pgen.1000889; PMID: 20361057
  • Guetg C, Lienemann P, Sirri V, Grummt I, Hernandez-Verdun D, Hottiger MO, Fussenegger M, Santoro R. The NoRC complex mediates the heterochromatin formation and stability of silent rRNA genes and centromeric repeats. EMBO J 2010; 29:2135 - 46; http://dx.doi.org/10.1038/emboj.2010.17; PMID: 20168299
  • Postepska-Igielska A, Krunic D, Schmitt N, Greulich-Bode KM, Boukamp P, Grummt I. The chromatin remodelling complex NoRC safeguards genome stability by heterochromatin formation at telomeres and centromeres. EMBO Rep 2013; 14:704 - 10; http://dx.doi.org/10.1038/embor.2013.87; PMID: 23797874
  • Diaz MO, Barsacchi-Pilone G, Mahon KA, Gall JG. Transcripts from both strands of a satellite DNA occur on lampbrush chromosome loops of the newt Notophthalmus. Cell 1981; 24:649 - 59; http://dx.doi.org/10.1016/0092-8674(81)90091-X; PMID: 6166385
  • Trapitz P, Wlaschek M, Bünemann H. Structure and function of Y chromosomal DNA. II. Analysis of lampbrush loop associated transcripts in nuclei of primary spermatocytes of Drosophila hydei by in situ hybridization using asymmetric RNA probes of four different families of repetitive DNA. Chromosoma 1988; 96:159 - 70; http://dx.doi.org/10.1007/BF00331048; PMID: 2450723
  • Rudert F, Bronner S, Garnier JM, Dollé P. Transcripts from opposite strands of gamma satellite DNA are differentially expressed during mouse development. Mamm Genome 1995; 6:76 - 83; http://dx.doi.org/10.1007/BF00303248; PMID: 7767009
  • Li YX, Kirby ML. Coordinated and conserved expression of alphoid repeat and alphoid repeat-tagged coding sequences. Dev Dyn 2003; 228:72 - 81; http://dx.doi.org/10.1002/dvdy.10355; PMID: 12950081
  • Martens JH, O’Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steinlein P, Jenuwein T. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 2005; 24:800 - 12; http://dx.doi.org/10.1038/sj.emboj.7600545; PMID: 15678104
  • Ferri F, Bouzinba-Segard H, Velasco G, Hubé F, Francastel C. Non-coding murine centromeric transcripts associate with and potentiate Aurora B kinase. Nucleic Acids Res 2009; 37:5071 - 80; http://dx.doi.org/10.1093/nar/gkp529; PMID: 19542185
  • Chan FL, Marshall OJ, Saffery R, Kim BW, Earle E, Choo KH, Wong LH. Active transcription and essential role of RNA polymerase II at the centromere during mitosis. Proc Natl Acad Sci U S A 2012; 109:1979 - 84; http://dx.doi.org/10.1073/pnas.1108705109; PMID: 22308327
  • Du Y, Topp CN, Dawe RK. DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA. PLoS Genet 2010; 6:e1000835; http://dx.doi.org/10.1371/journal.pgen.1000835; PMID: 20140237
  • Bergmann JH, Rodríguez MG, Martins NM, Kimura H, Kelly DA, Masumoto H, Larionov V, Jansen LE, Earnshaw WC. Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 2011; 30:328 - 40; http://dx.doi.org/10.1038/emboj.2010.329; PMID: 21157429
  • Bergmann JH, Jakubsche JN, Martins NM, Kagansky A, Nakano M, Kimura H, Kelly DA, Turner BM, Masumoto H, Larionov V, et al. Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function. J Cell Sci 2012; 125:411 - 21; http://dx.doi.org/10.1242/jcs.090639; PMID: 22331359
  • Maison C, Bailly D, Peters AH, Quivy JP, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet 2002; 30:329 - 34; http://dx.doi.org/10.1038/ng843; PMID: 11850619
  • Maison C, Bailly D, Roche D, Montes de Oca R, Probst AV, Vassias I, Dingli F, Lombard B, Loew D, Quivy JP, et al. SUMOylation promotes de novo targeting of HP1α to pericentric heterochromatin. Nat Genet 2011; 43:220 - 7; http://dx.doi.org/10.1038/ng.765; PMID: 21317888
  • Nakano M, Cardinale S, Noskov VN, Gassmann R, Vagnarelli P, Kandels-Lewis S, Larionov V, Earnshaw WC, Masumoto H. Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev Cell 2008; 14:507 - 22; http://dx.doi.org/10.1016/j.devcel.2008.02.001; PMID: 18410728
  • Bulut-Karslioglu A, Perrera V, Scaranaro M, de la Rosa-Velazquez IA, van de Nobelen S, Shukeir N, Popow J, Gerle B, Opravil S, Pagani M, et al. A transcription factor-based mechanism for mouse heterochromatin formation. Nat Struct Mol Biol 2012; 19:1023 - 30; http://dx.doi.org/10.1038/nsmb.2382; PMID: 22983563
  • Rizzi N, Denegri M, Chiodi I, Corioni M, Valgardsdottir R, Cobianchi F, Riva S, Biamonti G. Transcriptional activation of a constitutive heterochromatic domain of the human genome in response to heat shock. Mol Biol Cell 2004; 15:543 - 51; http://dx.doi.org/10.1091/mbc.E03-07-0487; PMID: 14617804
  • Biamonti G, Vourc’h C. Nuclear stress bodies. Cold Spring Harb Perspect Biol 2010; 2:a000695; http://dx.doi.org/10.1101/cshperspect.a000695; PMID: 20516127
  • Ting DT, Lipson D, Paul S, Brannigan BW, Akhavanfard S, Coffman EJ, Contino G, Deshpande V, Iafrate AJ, Letovsky S, et al. Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 2011; 331:593 - 6; http://dx.doi.org/10.1126/science.1200801; PMID: 21233348
  • Peters AH, O’Carroll D, Scherthan H, Mechtler K, Sauer S, Schöfer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 2001; 107:323 - 37; http://dx.doi.org/10.1016/S0092-8674(01)00542-6; PMID: 11701123
  • Palm W, de Lange T. How shelterin protects mammalian telomeres. Annu Rev Genet 2008; 42:301 - 34; http://dx.doi.org/10.1146/annurev.genet.41.110306.130350; PMID: 18680434
  • García-Cao M, O’Sullivan R, Peters AH, Jenuwein T, Blasco MA. Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet 2004; 36:94 - 9; http://dx.doi.org/10.1038/ng1278; PMID: 14702045
  • Benetti R, Gonzalo S, Jaco I, Schotta G, Klatt P, Jenuwein T, Blasco MA. Suv4-20h deficiency results in telomere elongation and derepression of telomere recombination. J Cell Biol 2007; 178:925 - 36; http://dx.doi.org/10.1083/jcb.200703081; PMID: 17846168
  • Nergadze SG, Farnung BO, Wischnewski H, Khoriauli L, Vitelli V, Chawla R, Giulotto E, Azzalin CM. CpG-island promoters drive transcription of human telomeres. RNA 2009; 15:2186 - 94; http://dx.doi.org/10.1261/rna.1748309; PMID: 19850908
  • Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007; 318:798 - 801; http://dx.doi.org/10.1126/science.1147182; PMID: 17916692
  • Schoeftner S, Blasco MA. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 2008; 10:228 - 36; http://dx.doi.org/10.1038/ncb1685; PMID: 18157120
  • Deng Z, Norseen J, Wiedmer A, Riethman H, Lieberman PM. TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol Cell 2009; 35:403 - 13; http://dx.doi.org/10.1016/j.molcel.2009.06.025; PMID: 19716786
  • Deng Z, Wang Z, Xiang C, Molczan A, Baubet V, Conejo-Garcia J, Xu X, Lieberman PM, Dahmane N. Formation of telomeric repeat-containing RNA (TERRA) foci in highly proliferating mouse cerebellar neuronal progenitors and medulloblastoma. J Cell Sci 2012; 125:4383 - 94; http://dx.doi.org/10.1242/jcs.108118; PMID: 22641694
  • Kazazian HH Jr.. Mobile elements: drivers of genome evolution. Science 2004; 303:1626 - 32; http://dx.doi.org/10.1126/science.1089670; PMID: 15016989
  • Faulkner GJ, Kimura Y, Daub CO, Wani S, Plessy C, Irvine KM, Schroder K, Cloonan N, Steptoe AL, Lassmann T, et al. The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 2009; 41:563 - 71; http://dx.doi.org/10.1038/ng.368; PMID: 19377475
  • Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 2007; 8:272 - 85; http://dx.doi.org/10.1038/nrg2072; PMID: 17363976
  • Lee E, Iskow R, Yang L, Gokcumen O, Haseley P, Luquette LJ 3rd, Lohr JG, Harris CC, Ding L, Wilson RK, et al, Cancer Genome Atlas Research Network. Landscape of somatic retrotransposition in human cancers. Science 2012; 337:967 - 71; http://dx.doi.org/10.1126/science.1222077; PMID: 22745252
  • Leung DC, Lorincz MC. Silencing of endogenous retroviruses: when and why do histone marks predominate?. Trends Biochem Sci 2012; 37:127 - 33; http://dx.doi.org/10.1016/j.tibs.2011.11.006; PMID: 22178137
  • Yang N, Kazazian HH Jr.. L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 2006; 13:763 - 71; http://dx.doi.org/10.1038/nsmb1141; PMID: 16936727
  • Ishizu H, Siomi H, Siomi MC. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev 2012; 26:2361 - 73; http://dx.doi.org/10.1101/gad.203786.112; PMID: 23124062
  • Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006; 442:203 - 7; PMID: 16751777
  • Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007; 128:1089 - 103; http://dx.doi.org/10.1016/j.cell.2007.01.043; PMID: 17346786
  • Deng W, Lin H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2002; 2:819 - 30; http://dx.doi.org/10.1016/S1534-5807(02)00165-X; PMID: 12062093
  • Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004; 131:839 - 49; http://dx.doi.org/10.1242/dev.00973; PMID: 14736746
  • Carmell MA, Girard A, van de Kant HJ, Bourc’his D, Bestor TH, de Rooij DG, Hannon GJ. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 2007; 12:503 - 14; http://dx.doi.org/10.1016/j.devcel.2007.03.001; PMID: 17395546
  • Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 2008; 31:785 - 99; http://dx.doi.org/10.1016/j.molcel.2008.09.003; PMID: 18922463
  • De Fazio S, Bartonicek N, Di Giacomo M, Abreu-Goodger C, Sankar A, Funaya C, Antony C, Moreira PN, Enright AJ, O’Carroll D. The endonuclease activity of Mili fuels piRNA amplification that silences LINE1 elements. Nature 2011; 480:259 - 63; http://dx.doi.org/10.1038/nature10547; PMID: 22020280
  • Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 2008; 22:908 - 17; http://dx.doi.org/10.1101/gad.1640708; PMID: 18381894
  • Fadloun A, Le Gras S, Jost B, Ziegler-Birling C, Takahashi H, Gorab E, Carninci P, Torres-Padilla ME. Chromatin signatures and retrotransposon profiling in mouse embryos reveal regulation of LINE-1 by RNA. Nat Struct Mol Biol 2013; 20:332 - 8; http://dx.doi.org/10.1038/nsmb.2495; PMID: 23353788
  • Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C, Davey NE, Humphreys DT, Preiss T, Steinmetz LM, et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 2012; 149:1393 - 406; http://dx.doi.org/10.1016/j.cell.2012.04.031; PMID: 22658674
  • Castello A, Horos R, Strein C, Fischer B, Eichelbaum K, Steinmetz LM, Krijgsveld J, Hentze MW. System-wide identification of RNA-binding proteins by interactome capture. Nat Protoc 2013; 8:491 - 500; http://dx.doi.org/10.1038/nprot.2013.020; PMID: 23411631

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.