Transcription of tandemly repetitive DNA: functional roles

Chromosome Research

Volumn 23, Issue 3, 2015, Pages 463-477

  Biscotti, Maria Assunta ^a   Canapa, Adriana ^a   Forconi, Mariko ^a   Olmo, Ettore ^a   Barucca, Marco ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Centromere; Centromeric transcription; Heterochromatin; Noncoding RNA; Pericentromeric transcription; Satellite DNA; Telomere; Telomeric transcription; TERRA

Indexed keywords

AURORA B KINASE; CENTROMERE PROTEIN A; DNA BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; LONG UNTRANSLATED RNA; PIWI PROTEIN; REPETITIVE DNA; REPLICATION FACTOR A; RNA DIRECTED RNA POLYMERASE; RNA INDUCED SILENCING COMPLEX; SATELLITE DNA; SMALL INTERFERING RNA; TELOMERASE REVERSE TRANSCRIPTASE; UNTRANSLATED RNA; DNA; HETEROCHROMATIN;

ARTICLE; CELL DIVISION; CELL STRESS; CENTROMERE; CHROMOSOME 9; CHROMOSOME PAIRING; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CONSTITUTIVE HETEROCHROMATIN; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; DNA TRANSCRIPTION; GENOMIC INSTABILITY; HETEROCHROMATIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; RNA INTERFERENCE; SISTER CHROMATID; TANDEM REPEAT; TELOMERE; TRANSCRIPTION TERMINATION; ANIMAL; EUKARYOTE; GENETIC PREDISPOSITION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; MOUSE; PHYSIOLOGICAL STRESS; TELOMERE HOMEOSTASIS;

ANIMALS; CENTROMERE; DNA; DNA, SATELLITE; EUKARYOTA; GENETIC PREDISPOSITION TO DISEASE; HETEROCHROMATIN; HUMANS; MICE; RNA, UNTRANSLATED; STRESS, PHYSIOLOGICAL; TANDEM REPEAT SEQUENCES; TELOMERE; TELOMERE HOMEOSTASIS; TRANSCRIPTION, GENETIC;

EID: 84947486368     PISSN: 09673849     EISSN: 15736849     Source Type: Journal    
DOI: 10.1007/s10577-015-9494-4     Document Type: Article

References (117)

1. Aldrup-Macdonald ME, Sullivan BA (2014) The past, present, and future of human centromere genomics. Genes (Basel) 5:33–50
2. Alexiadis V, Ballestas ME, Sanchez C, Winokur S, Vedanarayanan V, Warren M, Ehrlich M (2007) RNAPol-ChIP analysis of transcription from FSHD-linked tandem repeats and satellite DNA. Biochim Biophys Acta 1769:29–40
3. Arnoult N, VanBeneden A, Decottignies A (2012) Telomere length regulates TERRA levels through increased trimethylation of telomeric H3K9 and HP1 alpha. Nat Struct Mol Biol 19:948–956
4. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318:798–801
5. Bayne EH, White SA, Kagansky A, Bijos DA, Sanchez-Pulido L, Hoe KL, Kim DU, Park HO, Ponting CP, Rappsilber J, Allshire RC (2010) Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140:666–677
6. Bergmann JH, Jakubsche JN, Martins NM, Kagansky A, Nakano M, Kimura H, Kelly DA, Turner BM, Masumoto H, Larionov V, Earnshaw WC (2012) Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function. J Cell Sci 125:411–421
7. Blower MD, Sullivan BA, Karpen GH (2002) Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2:319–330
8. Bouzinba-Segard H, Guais A, Francastel C (2006) Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc Natl Acad Sci U S A 103:8709–8714
9. Broadbent KM, Park D, Wolf AR, Van Tyne D, Sims JS, Ribacke U, Volkman S, Duraisingh M, Wirth D, Sabeti PC, Rinn JL (2011) A global transcriptional analysis of Plasmodium falciparum malaria reveals a novel family of telomere-associated lncRNAs. Genome Biol 12:R56
10. Buker SM, Iida T, Bühler M, Villen J, Gygi SP, Nakayama J, Moazed D (2007) Two different Argonaute complexes are required for siRNA generation and heterochromatin assembly in fission yeast. Nat Struct Mol Biol 14:200–207
11. Bulazel KV, Ferreri GC, Eldridge MD, O'Neill RJ (2007) Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol 8:R170
12. Canapa A, Barucca M, Cerioni PN, Olmo E (2000) A satellite DNA containing CENP-B box-like motifs is present in the Antarctic scallop Adamussium colbecki. Gene 247:175–180
13. Caraballo DA, Belluscio PM, Rossi MS (2010) The library model for satellite DNA evolution: a case study with the rodents of the genus Ctenomys (Octodontidae) from the Iberá marsh, Argentina. Genetica 138:1201–1210
14. Cesari M, Luchetti A, Passamonti M, Scali V, Mantovani B (2003) Polymerase chain reaction amplification of the Bag320 satellite family reveals the ancestral library and past gene conversion events in Bacillus rossius (Insecta: Phasmatodea). Gene 312:289–295
15. Chan FL, Marshall OJ, Saffery R, Kim BW, Earle E, Choo KH, Wong LH (2012) Active transcription and essential role of RNA polymerase II at the centromere during mitosis. Proc Natl Acad Sci U S A 109:1979–1984
16. Chiodi I, Corioni M, Giordano M, Valgardsdottir R, Ghigna C, Cobianchi F, Xu RM, Riva S, Biamonti G (2004) RNA recognition motif 2 directs the recruitment of SF2/ASF to nuclear stress bodies. Nucleic Acids Res 32:4127–4136
17. Choi ES, Stralfors A, Catania S, Castillo AG, Svensson JP, Pidoux AL, Ekwall K, Allshire RC (2012) Factors that promote H3 chromatin integrity during transcription prevent promiscuous deposition of CENP-A(Cnp1) in fission yeast. PLoS Genet 8:e1002985
18. Choo KH (1997) The centromere. Oxford University Press, Oxford
19. Cusanelli E, Chartrand P (2014) Telomeric noncoding RNA: telomeric repeat-containing RNA in telomere biology. Wiley Interdiscip Rev RNA 5:407–419
20. Cusanelli E, Romero CAP, Chartrand P (2013) Telomeric noncoding RNA TERRA is induced by telomere shortening to nucleate telomerase molecules at short telomeres. Mol Cell 51:780–791
21. De La Fuente R, Baumann C, Viveiros MM (2015) ATRX contributes to epigenetic asymmetry and silencing of major satellite transcripts in the maternal genome of the mouse embryo. Development 142:1806–1817
22. Denegri M, Moralli D, Rocchi M, Biggiogera M, Raimondi E, Cobianchi F, De Carli L, Riva S, Biamonti G (2002) Human chromosomes 9, 12, and 15 contain the nucleation sites of stress-induced nuclear bodies. Mol Biol Cell 13:2069–2079
23. Deng Z, Norseen J, Wiedmer A, Riethman H, Lieberman PM (2009) TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol Cell 35:403–413
24. Deng Z, Wang Z, Stong N, Plasschaert R, Moczan A, Chen HS, Hu S, Wikramasinghe P, Davuluri RV, Bartolomei MS, Riethman H, Lieberman PM (2012) A role for CTCF and cohesin in subtelomere chromatin organization, TERRA transcription, and telomere end protection. EMBO J 31:4165–4178
25. Djupedal I, Kos-Braun IC, Mosher RA, Soderholm N, Simmer F, Hardcastle TJ, Fender A, Heidrich N, Kagansky A, Bayne E et al (2009) Analysis of small RNA in fission yeast; centromeric siRNAs are potentially generated through a structured RNA. EMBO J 28:3832–3844
26. Ehrlich M, Sanchez C, Shao C, Nishiyama R, Kehrl J, Kuick R, Kubota T, Hanash SM (2008) ICF, an immunodeficiency syndrome: DNA methyltransferase 3B involvement, chromosome anomalies, and gene dysregulation. Autoimmunity 41:253–271
27. Enukashvily NI, Ponomartsev NV (2013) Mammalian satellite DNA: a speaking dumb. Adv Protein Chem Struct Biol 90:31–65
28. Enukashvily N, Donev R, Waisertreiger IS, Podgornaya O (2007) Human chromosome 1 satellite 3 DNA is decondensed, demethylated and transcribed in senescent cells and in A431 epithelial carcinoma cells. Cytogenet Genome Res 118:42–54
29. Eymery A, Callanan M, Vourc'h C (2009a) The secret message of heterochromatin: new insights into the mechanisms and function of centromeric and pericentric repeat sequence transcription. Int J Dev Biol 53:259–268
30. Eymery A, Horard B, El Atifi-Borel M, Fourel G, Berger F, Vitte AL, Van den Broeck A, Brambilla E, Fournier A, Callanan M, Gazzeri S, Khochbin S, Rousseaux S, Gilson E, Vourc'h C (2009b) A transcriptomic analysis of human centromeric and pericentric sequences in normal and tumor cells. Nucleic Acids Res 37:6340–6354
31. Feliciello I, Akrap I, Ugarković Đ (2015) Satellite DNA modulates gene expression in the beetle Tribolium castaneum after heat stress. PLoS Genet 11:e1005466
32. Ferreira DP, Meles S, Escudeiro A, Mendes-da-Silva A, Adega F, Chaves R (2015) Satellite Noncoding RNAs: the emerging players in cells, cellular pathways and cancer. Chromosome Res. doi:10.1007/s10577-015-9482-8
33. Ferri F, Bouzinba-Segard H, Velasco G, Hube F, Francastel C (2009) Noncoding murine centromeric transcripts associate with and potentiate Aurora B kinase. Nucleic Acids Res 37:5071–5080
34. Flynn RL, Centore RC, O'Sullivan RJ, Rai R, Tse A, Songyang Z, Chang S, Karlseder J, Zou L (2011) TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature 471:532–536
35. Frescas D, Guardavaccaro D, Kuchay SM, Kato H, Poleshko A, Basrur V, Elenitoba-Johnson KS, Katz RA, Pagano M (2008) KDM2A represses transcription of centromeric satellite repeats and maintains the heterochromatic state. Cell Cycle 7:3539–3547
36. Fry K, Salser W (1977) Nucleotide sequences of HS-alpha satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 12:1069–1084
37. Fukagawa T, Nogami M, Yoshikawa M, Ikeno M, Okazaki T, Takami Y et al (2004) Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 6:784–791
38. Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10:94–108
39. Hall LE, Mitchell SE, O'Neill RJ (2012) Pericentric and centromeric transcription: a perfect balance required. Chromosome Res 20:535–546
40. Heitz E (1928) Das heterochromatin der moose. I Jahrb Wiss Botanik 69:762–818
41. Henikoff S, Dalal Y (2005) Centromeric chromatin: what makes it unique? Curr Opin Genet Dev 15:177–184
42. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox, stable inheritance with rapidly evolving DNA. Science 293:1098–1102
43. Heslop-Harrison JS, Brandes A, Schwarzacher T (2003) Tandemly repeated DNA sequences and centromeric chromosomal regions of Arabidopsis species. Chromosome Res 11:241–253
44. Holoch D, Moazed D (2015) RNA-mediated epigenetic regulation of gene expression. Nat Rev Genet 16:71–84
45. Hsieh CL, Lin CL, Liu H, Chang YJ, Shih CJ, Zhong CZ, Lee SC, Tan BC (2011) WDHD1 modulates the post-transcriptional step of the centromeric silencing pathway. Nucleic Acids Res 39:4048–4062
46. Ideue T, Cho Y, Nishimura K, Tani T (2014) Involvement of satellite I noncoding RNA in regulation of chromosome segregation. Genes Cells 19:528–538
47. Iida T, Nakayama J, Moazed D (2008) siRNA-mediated heterochromatin establishment requires HP1 and is associated with antisense transcription. Mol Cell 31:178–189
48. Jeanpierre M, Turleau C, Aurias A, Prieur M, Ledeist F, Fischer A, Viegas-Pequignot E (1993) An embryonic-like methylation pattern of classical satellite DNA is observed in ICF syndrome. Hum Mol Genet 2:731–735
49. Jolly C, Konecny L, Grady DL, Kutskova YA, Cotto JJ, Morimoto RI, Vourc’h C (2002) In vivo binding of active heat shock transcription factor 1 to human chromosome 9 heterochromatin during stress. J Cell Biol 156:775–781
50. Jolly C, Metz A, Govin J, Vigneron M, Turner BM, Khochbin S, Vourc’h C (2004) Stress-induced transcription of satellite III repeats. J Cell Biol 164:25–33
51. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19:489–501
52. Kowalik KM, Shimada Y, Flury V, Stadler MB, Batki J, Bühler M (2015) The Paf1 complex represses small-RNA-mediated epigenetic gene silencing. Nature 520:248–252
53. Kwon SH, Workman JL (2008) The heterochromatin protein 1 (HP1) family: put away a bias toward HP1. Mol Cells 26:217–227
54. Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120
55. Lippman Z, Martienssen R (2004) The role of RNA interference in heterochromatic silencing. Nature 431:364–370
56. Lorite P, Carrillo JA, Tinaut A, Palomeque T (2002) Comparative study of satellite DNA in ants of the Messor genus (Hymenoptera, Formicidae). Gene 297:113–122
57. Maida Y, Yasukawa M, Okamoto N, Ohka S, Kinoshita K, Totoki Y, Ito TK, Minamino T, Nakamura H, Yamaguchi S, Shibata T, Masutomi K (2014) Involvement of telomerase reverse transcriptase in heterochromatin maintenance. Mol Cell Biol 34:1576–1593
58. Martin C, Zhang Y (2005) The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 6:838–849
59. Martínez-Lage A, Rodríguez-Fariña F, González-Tizón A, Méndez J (2005) Origin and evolution of Mytilus mussel satellite DNAs. Genome 48:247–256
60. Masumoto H, Masukata H, Muro Y, Nozaki N, Okazaki T (1989) A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite. J Cell Biol 109:1963–1973
61. Meštrović N, Plohl M, Mravinac B, Ugarković D (1998) Evolution of satellite DNAs from the genus Palorus—experimental evidence for the “library” hypothesis. Mol Biol Evol 15:1062–1068
62. Meštrović N, Castagnone-Sereno P, Plohl M (2006) Interplay of selective pressure and stochastic events directs evolution of the MEL172 satellite DNA library in root-knot nematodes. Mol Biol Evol 23:2316–2325
63. Meštrović N, Pavlek M, Car A, Castagnone-Sereno P, Abad P, Plohl M (2013) Conserved DNA motifs, including the CENP-B Box-like, are possible promoters of satellite DNA array rearrangements in nematodes. PLoS One 8:e67328
64. Metz A, Soret J, Vourc’h C, Tazi J, Jolly C (2004) A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules. J Cell Sci 117:4551–4558
65. Michalik KM, Bottcher R, Forstemann K (2012) A small RNA response at DNA ends in Drosophila. Nucleic Acids Res 40:9596–9603
66. Motamedi MR, Verdel A, Colmenares SU, Gerber SA, Gygi SP, Moazed D (2004) Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119:789–802
67. Mravinać B, Plohl M, Ugarković D (2005) Preservation and high sequence conservation of satellite DNAs suggest functional constraints. J Mol Evol 61:542–550
68. Neumann P, Yan H, Jiang J (2007) The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference. Genetics 176:749–761
69. Noh KM, Maze I, Zhao D, Xiang B, Wenderski W, Lewis PW, Shen L, Li H, Allis CD (2015) ATRX tolerates activity-dependent histone H3 methyl/phos switching to maintain repetitive element silencing in neurons. Proc Natl Acad Sci U S A 112:6820–6827
70. Ohkuni K, Kitagawa K (2011) Endogenous transcription at the centromere facilitates centromere activity in budding yeast. Curr Biol 21:1695–1703
71. Ohno (1972) So much “junk” DNA in our genome. Brookhaven Symp Biol 23:366–370
72. Okada M, Okawa K, Isobe T, Fukagawa T (2009) CENP-H-containing complex facilitates centromere deposition of CENP-A in cooperation with FACT and CHD1. Mol Biol Cell 20:3986–3995
73. O'Sullivan RJ, Karlseder J (2010) Telomeres: protecting chromosomes against genome instability. Nat Rev Mol Cell Biol 11:171–181
74. Palazzo AF, Gregory TR (2014) The case for junk DNA. PLoS Genet 10:e1004351
75. Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Mittelsten Scheid O (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22:3118–3129
76. Pennisi E (2010) Shining a light on the genome’s ‘dark matter’. Science 330:1614
77. Petraccioli A, Odierna G, Capriglione T, Barucca M, Forconi M, Olmo E, Biscotti MA (2015) A novel satellite DNA isolated in Pecten jacobaeus shows high sequence similarity among molluscs. Mol Gen and Genom. doi:10.1007/s00438-015-1036-4
78. Pezer Z, Ugarković D (2008) Role of non-coding RNA and heterochromatin in aneuploidy and cancer. Semin Cancer Biol 18:123–130
79. Pezer Z, Ugarkovic D (2012) Satellite DNA-associated siRNAs as mediators of heat shock response in insects. RNA Biol 9:587–595
80. Pezer Z, Brajković J, Feliciello I, Ugarkovć D (2012) Satellite DNA-mediated effects on genome regulation. Genome Dyn 7:153–169
81. Pfeiffer V, Crittin J, Grolimund L, Lingner J (2013) The THO complex component Thp2 counteracts telomeric R-loops and telomere shortening. EMBO J 32:2861–2871
82. Plohl M, Luchetti A, Mestrovic N, Mantovani B (2008) Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene 409:72–82
83. Plohl M, Meštrović N, Mravinac B (2012) Satellite DNA evolution. Genome Dyn 7:126–152
84. Porro A, Feuerhahn S, Reichenbach P, Lingner J (2010) Molecular dissection of telomeric repeat-containing RNA biogenesis unveils the presence of distinct and multiple regulatory pathways. Mol Cell Biol 30:4808–4817
85. Porro A, Feuerhahn S, Delafontaine J, Riethman H, RougemontJ LJ (2014) FunctionalcharacterizationoftheTERRA transcriptome at damaged telomeres. Nat Commun 5:5379
86. Postepska-Igielska A, Krunic D, Schmitt N, Greulich-Bode KM, Boukamp P, Grummt I (2013) The chromatin remodelling complex NoRC safeguards genome stability by heterochromatin formation at telomeres and centromeres. EMBO Rep 14:704–710
87. Probst AV, Okamoto I, Casanova M, El Marjou F, Le Baccon P, Almouzni G (2010) A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell 19:625–638
88. Prokocimer M, Barkan R, Gruenbaum Y (2013) Hutchinson-Gilford progeria syndrome through the lens of transcription. Aging Cell 12:533–43
89. Quénet D, Dalal Y (2014) A long noncoding RNA is required for targeting centromeric protein A to the human centromere. Elife 3:e03254
90. Redon S, Reichenbach P, Lingner J (2010) The noncoding RNA TERRA is a natural ligand and direct inhibitor of human telomerase. Nucleic Acids Res 38:5797–5806
91. Rizzi N, Denegri M, Chiodi I, Corioni M, Valgardsdottir R, Cobianchi F, Riva S, Biamonti G (2004) Transcriptional activation of a constitutive heterochromatic domain of the human genome in response to heat shock. Mol Biol Cell 15:543–551
92. Rošić S, Köhler F, Erhardt S (2014) Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division. J Cell Biol 207:335–349
93. Saffery R, Sumer H, Hassan S, Wong LH, Craig JM, Todokoro K, Anderson M, Stafford A, Choo KH (2003) Transcription within a functional human centromere. Mol Cell 12:509–516
94. Saksouk N, Barth TK, Ziegler-Birling C, Olova N, Nowak A, Rey E, Mateos-Langerak J, Urbach S, Reik W, Torres-Padilla ME, Imhof A, Déjardin J, Simboeck E (2014) Redundant mechanisms to form silent chromatin at pericentromeric regions rely on BEND3 and DNA methylation. Mol Cell 56:580–594
95. Saksouk N, Simboeck E, Déjardin J (2015) Constitutive heterochromatin formation and transcription in mammals. Epigenetics Chromatin 8:3
96. Schoeftner S, Blasco MA (2008) Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 10:228–236
97. Schoeftner S, Blasco MA (2009) A ‘higher order’ of telomere regulation: telomere heterochromatin and telomeric RNAs. EMBO J 28:2323–2336
98. Shapiro JA, von Sternberg R (2005) Why repetitive DNA is essential to genome function. Biol Rev Camb Philos Soc 80:227–250
99. Shumaker DK, Dechat T, Kohlmaier A, Adam SA, Bozovsky MR, Erdos MR, Eriksson M, Goldman AE, Khuon S, Collins FS, Jenuwein T, Goldman RD (2006) Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc Natl Acad Sci U S A 103:8703–8708
100. Slamovits CH, Cook JA, Lessa EP, Rossi MS (2001) Recurrent amplifications and deletions of satellite DNA accompanied chromosomal diversification in South American tuco-tucos (genus Ctenomys, Rodentia: Octodontidae): a phylogenetic approach. Mol Biol Evol 18:1708–1719
101. Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, Cohen TV, Devys D, Foisner R, Peichl L, Herrmann H, Blum H, Engelkamp D, Stewart CL, Leonhardt H, Joffe B (2013) LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152:584–598
102. Sugimura K, Fukushima Y, Ishida M, Ito S, Nakamura M, Mori Y, Okumura K (2010) Cell cycle-dependent accumulation of histone H3.3 and euchromatic histone modifications in pericentromeric heterochromatin in response to a decrease in DNA methylation levels. Exp Cell Res 316:2731–2746
103. Ting DT, Lipson D, Paul S, Brannigan BW, Akhavanfard S, Coffman EJ, Contino G, Deshpande V, Iafrate AJ, Letovsky S, Rivera MN, Bardeesy N, Maheswaran S, Haber DA (2011) Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 331:593–596
104. Tittel-Elmer M, Bucher E, Broger L, Mathieu O, Paszkowski J, Vaillant I (2010) Stress-induced activation of heterochromatic transcription. PLoS Genet 6:e1001175
105. Towbin BD, González-Aguilera C, Sack R, Gaidatzis D, Kalck V, Meister P, Askjaer P, Gasser SM (2012) Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150:934–947
106. Ugarković D (2005) Functional elements residing within satellite. DNAs EMBO Rep 6:1035–1039
107. Valgardsdottir R, Chiodi I, Giordano M, Rossi A, Bazzini S, Ghigna C, Riva S, Biamonti G (2008) Transcription of Satellite III noncoding RNAs is a general stress response in human cells. Nucleic Acids Res 36:423–434
108. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672–676
109. Vittorazzi S, Lourenço L, Recco-Pimentel S (2014) Long-time evolution and highly dynamic satellite DNA in leptodactylid and hylodid frogs. BMC Genet 15:111
110. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833–1837
111. Wang C, Zhao L, Lu S (2015) Role of TERRA in the regulation of telomere length. Int J Biol Sci 11:316–323
112. Wei W, Ba Z, Gao M, Wu Y, Ma Y, Amiard S, White CI, Rendtlew Danielsen JM, Yang YG, Qi Y (2012) A role for small RNAs in DNA double-strand break repair. Cell 149:101–112
113. Wilson AS, Power BE, Molloy PL (2007) DNA hypomethylation and human diseases. Biochim Biophys Acta 1775:138–162
114. Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, Northrop EL, Hannan R, Saffery R, Shaw ML, Williams E et al (2007) Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res 17:1146–1160
115. Yang Q, Ye QA, Liu Y (2015) Mechanism of siRNA production from repetitive DNA. Genes Dev 29:526–537
116. Zhang K, Mosch K, Fischle W, Grewal SI (2008) Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat Struct Mol Biol 15:381–388
117. Zhu Q, Pao GM, Huynh AM, Suh H, Tonnu N, Nederlof PM, Gage FH, Verma IM (2011) BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 477:179–184