Genomic relationship between SINE retrotransposons, Pol III-Pol II transcription, and chromatin organization: The journey from junk to jewel

Biochemistry and Cell Biology

Volumn 89, Issue 5, 2011, Pages 495-504

  Lunyak, Victoria V ^a   Atallah, Michelle ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

Chromatin architecture; Genomic boundaries; Intrachromosomal interactions; Pol III transcription; Retrotransposons; SINE; TFIIIC; TRNA genes

Indexed keywords

CHROMATIN ARCHITECTURE; GENOMIC BOUNDARIES; INTRACHROMOSOMAL INTERACTIONS; POL III TRANSCRIPTION; RETROTRANSPOSONS; SINE; TFIIIC; TRNA GENES;

MAMMALS; RNA; TRANSCRIPTION;

GENES;

DNA DIRECTED RNA POLYMERASE III; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSFER RNA;

CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC TRANSCRIPTION; GENOME; HUMAN; LONG INTERSPERSED REPEAT; LONG TERMINAL REPEAT; MAMMAL; NONHUMAN; PROTEIN BINDING; RETROPOSON; REVIEW; SHORT INTERSPERSED REPEAT;

ANIMALS; CHROMATIN; DNA POLYMERASE II; DNA POLYMERASE III; GENOME; HUMANS; MICE; RETROELEMENTS; SHORT INTERSPERSED NUCLEOTIDE ELEMENTS;

EUKARYOTA; MAMMALIA;

EID: 80053990356     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/o11-046     Document Type: Review

References (98)

1. Amaral P.P. Dinger M.E. Mercer T.R. Mattick J.S. 2008. The eukaryotic genome as an RNA machine. Science (Washington, D.C.), 319 (5871): 1787-1789. 10.1126/science.1155472 18369136 (Pubitemid 351451554)
2. Arnaud P. Goubely C. Pelissier T. Deragon J.M. 2000. SINE retroposons can be used in vivo as nucleation centers for de novo methylation. Mol. Cell. Biol. 20 (10): 3434-3441. 10.1128/MCB.20.10.3434-3441.2000 10779333 (Pubitemid 30243889)
3. Barski A. Chepelev I. Liko D. Cuddapah S. Fleming A.B. Birch J. et al. 2010. Pol II and its associated epigenetic marks are present at Pol III-transcribed noncoding RNA genes. Nat. Struct. Mol. Biol. 17 (5): 629-634. 10.1038/nsmb.1806 20418881
4. Batzer M.A. Schmid C.W. Deininger P.L. 1993. Evolutionary analyses of repetitive DNA sequences. Methods Enzymol. 224: 213-232. 10.1016/0076-6879(93) 24017-O 8264388
5. Bennett K.L. Hill R.E. Pietras D.F. Woodworth-Gutai M. Kane-Haas C. Houston J.M. et al. 1984. Most highly repeated dispersed DNA families in the mouse genome. Mol. Cell. Biol. 4 (8): 1561-1571. 6208477 (Pubitemid 15131917)
6. Boeke J.D. 1997. LINEs and Alus ' the polyA connection. Nat. Genet. 16 (1): 6-7. 10.1038/ng0597-6 9140383
7. Borchert G.M. Lanier W. Davidson B.L. 2006. RNA polymerase III transcribes human microRNAs. Nat. Struct. Mol. Biol. 13 (12): 1097-1101. 10.1038/nsmb1167 17099701 (Pubitemid 44885920)
8. Bourque G. 2009. Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr. Opin. Genet. Dev. 19 (6): 607-612. 10.1016/j.gde.2009.10.013 19914058
9. Bourque G. Leong B. Vega V.B. Chen X. Lee Y.L. Srinivasan K.G. et al. 2008. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res. 18 (11): 1752-1762. 10.1101/gr.080663.108 18682548
10. Chandler V.L. Walbot V. 1986. DNA modification of a maize transposable element correlates with loss of activity. Proc. Natl. Acad. Sci. U.S.A. 83 (6): 1767-1771. 10.1073/pnas.83.6.1767 3006070 (Pubitemid 16018644)
11. Chinwalla A.T. Delehaunty K.D. Fewell G.A. Fulton L.A. Fulton R.S. Graves T.A. et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature (Lond.), 420 (6915): 520-562. 10.1038/nature01262 12466850 (Pubitemid 35477048)
12. Chédin S. Riva M. Schultz P. Sentenac A. Carles C. 1998. The RNA cleavage activity of RNA polymerase III is mediated by an essential TFIIS-like subunit and is important for transcription termination. Genes Dev. 12 (24): 3857-3871. 10.1101/gad.12.24.3857 9869639 (Pubitemid 29024848)
13. Chow J.C. Ciaudo C. Fazzari M.J. Mise N. Servant N. Glass J.L. et al. 2010. LINE-1 activity in facultative heterochromatin formation during X chromosome inactivation. Cell, 141 (6): 956-969. 10.1016/j.cell.2010.04.042 20550932
14. Chugani D.C. Rome L.H. Kedersha N.L. 1993. Evidence that vault ribonucleoprotein particles localize to the nuclear pore complex. J. Cell Sci. 106 (Pt. 1): 23-29. 8270627 (Pubitemid 23286775)
15. Coufal N.G. Garcia-Perez J.L. Peng G.E. Yeo G.W. Mu Y. Lovci M.T. et al. 2009. L1 retrotransposition in human neural progenitor cells. Nature (Lond.), 460 (7259): 1127-1131. 10.1038/nature08248 19657334
16. D'Ambrosio C. Schmidt C.K. Katou Y. Kelly G. Itoh T. Shirahige K. Uhlmann F. 2008 a. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev. 22 (16): 2215-2227. 10.1101/gad.1675708 18708580
17. D'Ambrosio C. Kelly G. Shirahige K. Uhlmann F. 2008 b. Condensin-dependent rDNA decatenation introduces a temporal pattern to chromosome segregation. Curr. Biol. 18 (14): 1084-1089. 10.1016/j.cub.2008.06. 058 18635352
18. Damert A. Raiz J. Horn A.V. Löwer J. Wang H. Xing J. et al. 2009. 5′-Transducing SVA retrotransposon groups spread efficiently throughout the human genome. Genome Res. 19 (11): 1992-2008. 10.1101/gr.093435.109 19652014
19. Dean N. Berk A.J. 1987. Separation of TFIIIC into two functional components by sequence specific DNA affinity chromatography. Nucleic Acids Res. 15 (23): 9895-9907. 10.1093/nar/15.23.9895 3697084
20. Deng W. Zhu X. Skogerbø G. Zhao Y. Fu Z. Wang Y. et al. 2006. Organization of the Caenorhabditis elegans small non-coding transcriptome: genomic features, biogenesis, and expression. Genome Res. 16 (1): 20-29. 10.1101/gr.4139206 16344563 (Pubitemid 43048930)
21. Deshpande A.M. Newlon C.S. 1996. DNA replication fork pause sites dependent on transcription. Science (Washington, D.C.), 272 (5264): 1030-1033. 10.1126/science.272.5264.1030 8638128 (Pubitemid 26259324)
22. Dhillon N. Raab J. Guzzo J. Szyjka S.J. Gangadharan S. Aparicio O.M. et al. 2009. DNA polymerase epsilon, acetylases and remodellers cooperate to form a specialized chromatin structure at a tRNA insulator. EMBO J. 28 (17): 2583-2600. 10.1038/emboj.2009.198 19629037
23. Dieci G. Fiorino G. Castelnuovo M. Teichmann M. Pagano A. 2007. The expanding RNA polymerase III transcriptome. Trends Genet. 23 (12): 614-622. 10.1016/j.tig.2007.09.001 17977614 (Pubitemid 350180140)
24. Donze D. Adams C.R. Rine J. Kamakaka R.T. 1999. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev. 13 (6): 698-708. 10.1101/gad.13.6.698 10090726 (Pubitemid 29155976)
25. Dumay-Odelot H. Marck C. Durrieu-Gaillard S. Lefebvre O. Jourdain S. Prochazkova M. et al. 2007. Identification, molecular cloning, and characterization of the sixth subunit of human transcription factor TFIIIC. J. Biol. Chem. 282 (23): 17179-17189. 10.1074/jbc.M611542200 17409385 (Pubitemid 47093196)
26. Dumay-Odelot H. Durrieu-Gaillard S. Da Silva D. Roeder R.G. Teichmann M. 2010. Cell growth-and differentiation-dependent regulation of RNA polymerase III transcription. Cell Cycle, 9 (18): 3687-3699. 10.4161/cc.9.18.13203 20890107
27. Englander E.W. Wolffe A.P. Howard B.H. 1993. Nucleosome interactions with a human Alu element. Transcriptional repression and effects of template methylation. J. Biol. Chem. 268 (26): 19565-19573. 8366099 (Pubitemid 23270742)
28. Faulkner G.J. Kimura Y. Daub C.O. Wani S. Plessy C. Irvine K.M. et al. 2009. The regulated retrotransposon transcriptome of mammalian cells. Nat. Genet. 41 (5): 563-571. 10.1038/ng.368 19377475
29. Feng Q. Moran J.V. Kazazian H.H. Jr Boeke J.D. 1996. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell, 87 (5): 905-916. 10.1016/S0092-8674(00)81997-2 8945517 (Pubitemid 26404289)
30. Fernández-Tornero C. Böttcher B. Riva M. Carles C. Steuerwald U. Ruigrok R.W. et al. 2007. Insights into transcription initiation and termination from the electron microscopy structure of yeast RNA polymerase III. Mol. Cell, 25 (6): 813-823. 10.1016/j.molcel.2007.02.016 17386259 (Pubitemid 46442793)
31. Ferrigno O. Virolle T. Djabari Z. Ortonne J.P. White R.J. Aberdam D. 2001. Transposable B2 SINE elements can provide mobile RNA polymerase II promoters. Nat. Genet. 28 (1): 77-81. 10.1038/ng0501-77 11326281 (Pubitemid 32405822)
32. Geiduschek E.P. Kassavetis G.A. 2001. The RNA polymerase III transcription apparatus. J. Mol. Biol. 310 (1): 1-26. 10.1006/jmbi.2001.4732 11419933 (Pubitemid 32621715)
33. Giuliodori S. Percudani R. Braglia P. Ferrari R. Guffanti E. Ottonello S. Dieci G. 2003. A composite upstream sequence motif potentiates tRNA gene transcription in yeast. J. Mol. Biol. 333 (1): 1-20. 10.1016/j.jmb.2003.08.016 14516739 (Pubitemid 37153261)
34. Good P.D. Krikos A.J. Li S.X. Bertrand E. Lee N.S. Giver L. et al. 1997. Expression of small, therapeutic RNAs in human cell nuclei. Gene Ther. 4 (1): 45-54. 10.1038/sj.gt.3300354 9068795 (Pubitemid 27073222)
35. Goodrich J.A. Kugel J.F. 2006. Non-coding-RNA regulators of RNA polymerase II transcription. Nat. Rev. Mol. Cell Biol. 7 (8): 612-616. 10.1038/nrm1946 16723972 (Pubitemid 44325352)
36. Haeusler R.A. Engelke D.R. 2006. Spatial organization of transcription by RNA polymerase III. Nucleic Acids Res. 34 (17): 4826-4836. 10.1093/nar/gkl656 16971453 (Pubitemid 44607803)
37. Haeusler R.A. Pratt-Hyatt M. Good P.D. Gipson T.A. Engelke D.R. 2008. Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes Dev. 22 (16): 2204-2214. 10.1101/gad.1675908 18708579
38. Han K. Lee J. Meyer T.J. Remedios P. Goodwin L. Batzer M.A. 2008. L1 recombination-associated deletions generate human genomic variation. Proc. Natl. Acad. Sci. U.S.A. 105 (49): 19366-19371. 10.1073/pnas.0807866105 19036926
39. Hasse A. Schulz W.A. 1994. Enhancement of reporter gene de novo methylation by DNA fragments from the α-fetoprotein control region. J. Biol. Chem. 269 (3): 1821-1826. 7507485 (Pubitemid 24035379)
40. Hsieh Y.J. Wang Z. Kovelman R. Roeder R.G. 1999 a. Cloning and characterization of two evolutionarily conserved subunits (TFIIIC102 and TFIIIC63) of human TFIIIC and their involvement in functional interactions with TFIIIB and RNA polymerase III. Mol. Cell. Biol. 19 (7): 4944-4952. 10373544 (Pubitemid 29289533)
41. Hsieh Y.J. Kundu T.K. Wang Z. Kovelman R. Roeder R.G. 1999 b. The TFIIIC90 subunit of TFIIIC interacts with multiple components of the RNA polymerase III machinery and contains a histone-specific acetyltransferase activity. Mol. Cell. Biol. 19 (11): 7697-7704. 10523658 (Pubitemid 29493433)
42. Huang Y. Maraia R.J. 2001. Comparison of the RNA polymerase III transcription machinery in Schizosaccharomyces pombe, Saccharomyces cerevisiae and human. Nucleic Acids Res. 29 (13): 2675-2690. 10.1093/nar/29.13.2675 11433012 (Pubitemid 32685030)
43. Kaplan F.S. Murray J. Sylvester J.E. Gonzalez I.L. O'Connor J.P. Doering J.L. et al. 1993. The topographic organization of repetitive DNA in the human nucleolus. Genomics, 15 (1): 123-132. 10.1006/geno.1993.1020 8432523 (Pubitemid 23079581)
44. Kelter A.R. Herchenbach J. Wirth B. 2000. The transcription factor-like nuclear regulator (TFNR) contains a novel 55-amino-acid motif repeated nine times and maps closely to SMN1. Genomics, 70 (3): 315-326. 10.1006/geno.2000. 6396 11161782 (Pubitemid 32095430)
45. Kidd J.M. Cooper G.M. Donahue W.F. Hayden H.S. Sampas N. Graves T. et al. 2008. Mapping and sequencing of structural variation from eight human genomes. Nature (Lond.), 453 (7191): 56-64. 10.1038/nature06862 18451855 (Pubitemid 351630326)
46. Kovelman R. Roeder R.G. 1992. Purification and characterization of two forms of human transcription factor IIIC. J. Biol. Chem. 267 (34): 24446-24456. 1447193
47. Kramerov D.A. Vassetzky N.S. 2005. Short retroposons in eukaryotic genomes. Int. Rev. Cytol. 247: 165-221. 10.1016/S0074-7696(05)47004-7 16344113 (Pubitemid 41774365)
48. Kundu T.K. Wang Z. Roeder R.G. 1999. Human TFIIIC relieves chromatin-mediated repression of RNA polymerase III transcription and contains an intrinsic histone acetyltransferase activity. Mol. Cell. Biol. 19 (2): 1605-1615. 9891093 (Pubitemid 29046901)
49. Lander E.S. Linton L.M. Birren B. Nusbaum C. Zody M.C. Baldwin J. et al. 2001. Initial sequencing and analysis of the human genome. Nature (Lond.), 409 (6822): 860-921. 10.1038/35057062 11237011 (Pubitemid 32165345)
50. Landrieux E. Alic N. Ducrot C. Acker J. Riva M. Carles C. 2006. A subcomplex of RNA polymerase III subunits involved in transcription termination and reinitiation. EMBO J. 25 (1): 118-128. 10.1038/sj.emboj.7600915 16362040 (Pubitemid 43077301)
51. Lin C. Yang L. Tanasa B. Hutt K. Ju B.G. Ohgi K. et al. 2009. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell, 139 (6): 1069-1083. 10.1016/j.cell.2009.11.030 19962179
52. Lunyak V.V. 2008. Boundaries. Boundaries-Boundaries. Curr. Opin. Cell Biol. 20 (3): 281-287. 10.1016/j.ceb.2008.03.018 18524562
53. Lunyak V.V. Prefontaine G.G. Núñez E. Cramer T. Ju B.G. Ohgi K.A. et al. 2007. Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science, 317 (5835): 248-251. 10.1126/science.1140871 17626886 (Pubitemid 47076201)
54. Martignetti J.A. Brosius J. 1993. BC200 RNA: a neural RNA polymerase III product encoded by a monomeric Alu element. Proc. Natl. Acad. Sci. U.S.A. 90 (24): 11563-11567. 10.1073/pnas.90.24.11563 8265590 (Pubitemid 24008679)
55. Martignetti J.A. Brosius J. 1995. BC1 RNA: transcriptional analysis of a neural cell-specific RNA polymerase III transcript. Mol. Cell. Biol. 15 (3): 1642-1650. 7862155
56. McClintock B. 1956. Controlling elements and the gene. Cold Spring Harb. Symp. Quant. Biol. 21: 197-216. 13433592
57. Mittal V. Ma B. Hernandez N. 1999. SNAP(c): a core promoter factor with a built-in DNA-binding damper that is deactivated by the Oct-1 POU domain. Genes Dev. 13 (14): 1807-1821. 10.1101/gad.13.14.1807 10421633 (Pubitemid 29353048)
58. Moqtaderi Z. Wang J. Raha D. White R.J. Snyder M. Weng Z. Struhl K. 2010. Genomic binding profiles of functionally distinct RNA polymerase III transcription complexes in human cells. Nat. Struct. Mol. Biol. 17 (5): 635-640. 10.1038/nsmb.1794 20418883
59. Morrish T.A. Gilbert N. Myers J.S. Vincent B.J. Stamato T.D. Taccioli G.E. et al. 2002. DNA repair mediated by endonuclease-independent LINE-1 retrotransposition. Nat. Genet. 31 (2): 159-165. 10.1038/ng898 12006980
60. Muotri A.R. Chu V.T. Marchetto M.C.N. Deng W. Moran J.V. Gage F.H. 2005. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature (Lond.), 435 (7044): 903-910. 10.1038/nature03663 15959507 (Pubitemid 40896309)
61. Muotri A.R. Marchetto M.C. Coufal N.G. Gage F.H. 2007. The necessary junk: new functions for transposable elements. Hum. Mol. Genet. 16 (R2): R159-R167. 10.1093/hmg/ddm196 17911158
62. Muslimov I.A. Lin Y. Heller M. Brosius J. Zakeri Z. Tiedge H. 2002. A small RNA in testis and brain: implications for male germ cell development. J. Cell Sci. 115 (Pt. 6): 1243-1250. 11884523 (Pubitemid 34272488)
63. Nguyen V.T. Kiss T. Michels A.A. Bensaude O. 2001. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature (Lond.), 414 (6861): 322-325. 10.1038/35104581 11713533 (Pubitemid 33097810)
64. Noma K. Cam H.P. Maraia R.J. Grewal S.I. 2006. A role for TFIIIC transcription factor complex in genome organization. Cell, 125 (5): 859-872. 10.1016/j.cell.2006.04.028 16751097 (Pubitemid 43795193)
65. Oettel S. Hartel F. Kober I. Iben S. Seifart K.H. 1997. Human transcription factors IIIC2, IIIC1 and a novel component IIIC0 fulfil different aspects of DNA binding to various pol III genes. Nucleic Acids Res. 25 (12): 2440-2447. 10.1093/nar/25.12.2440 9171097 (Pubitemid 27303705)
66. Okada N. 1991. SINEs. Curr. Opin. Genet. Dev. 1 (4): 498-504. 10.1016/S0959-437X(05)80198-4 1668310
67. Oki M. Kamakaka R.T. 2005. Barrier function at HMR. Mol. Cell, 19 (5): 707-716. 10.1016/j.molcel.2005.07.022 16137626 (Pubitemid 41219446)
68. Oler A.J. Alla R.K. Roberts D.N. Wong A. Hollenhorst P.C. Chandler K.J. et al. 2010. Human RNA polymerase III transcriptomes and relationships to Pol II promoter chromatin and enhancer-binding factors. Nat. Struct. Mol. Biol. 17 (5): 620-628. 10.1038/nsmb.1801 20418882
69. Pai D.A. Engelke D.R. 2010. Spatial organization of genes as a component of regulated expression. Chromosoma, 119 (1): 13-25. 10.1007/s00412-009-0236-2 19727792
70. Parrott A.M. Walsh M.R. Mathews M.B. 2007. Analysis of RNA:protein interactions in vivo: identification of RNA-binding partners of nuclear factor 90. Methods Enzymol. 429: 243-260. 10.1016/S0076-6879(07)29012-3 17913627
71. Paule M.R. White R.J. 2000. Survey and summary: transcription by RNA polymerases I and III. Nucleic Acids Res. 28 (6): 1283-1298. 10.1093/nar/28.6.1283 10684922 (Pubitemid 30142670)
72. Paulson K.E. Deka N. Schmid C.W. Misra R. Schindler C.W. Rush M.G. et al. 1985. A transposon-like element in human DNA. Nature (Lond.), 316 (6026): 359-361. 10.1038/316359a0 2862587 (Pubitemid 15237812)
73. Perlman P.S. Boeke J.D. 2004. Molecular biology. Ring around the retroelement. Science (Washington, D.C.), 303 (5655): 182-184. 10.1126/science.1093514 14716001 (Pubitemid 38057559)
74. Pombo A. Jackson D.A. Hollinshead M. Wang Z. Roeder R.G. Cook P.R. 1999. Regional specialization in human nuclei: visualization of discrete sites of transcription by RNA polymerase III. EMBO J. 18 (8): 2241-2253. 10.1093/emboj/18.8.2241 10205177 (Pubitemid 29179180)
75. Ponicsan S.L. Kugel J.F. Goodrich J.A. 2010. Genomic gems: SINE RNAs regulate mRNA production. Curr. Opin. Genet. Dev. 20 (2): 149-155. 10.1016/j.gde.2010.01.004 20176473
76. Raab J.R. Kamakaka R.T. 2010. Insulators and promoters: closer than we think. Nat. Rev. Genet. 11 (6): 439-446. 10.1038/nrg2765 20442713
77. Roman A.C. Benitez D.A. Carvajal-Gonzalez J.M. Fernandez-Salguero P.M. 2008. Genome-wide B1 retrotransposon binds the transcription factors dioxin receptor and Slug and regulates gene expression in vivo. Proc. Natl. Acad. Sci. U.S.A. 105 (5): 1632-1637. 10.1073/pnas.0708366105 18223155 (Pubitemid 351346566)
78. Román A.C. González-Rico F.J. Moltó E. Hernando H. Neto A. Vicente-Garcia C. et al. 2011. Dioxin receptor and SLUG transcription factors regulate the insulator activity of B1 SINE retrotransposons via an RNA polymerase switch. Genome Res. 21 (3): 422-432. 10.1101/gr.111203.110 21324874
79. Schaub M. Myslinski E. Schuster C. Krol A. Carbon P. 1997. Staf, a promiscuous activator for enhanced transcription by RNA polymerases II and III. EMBO J. 16 (1): 173-181. 10.1093/emboj/16.1.173 9009278 (Pubitemid 27032860)
80. Schramm L. Hernandez N. 2002. Recruitment of RNA polymerase III to its target promoters. Genes Dev. 16 (20): 2593-2620. 10.1101/gad.1018902 12381659
81. Smit A.F. Toth G. Riggs A.D. Jurka J. 1995. Ancestral, mammalian-wide subfamilies of LINE-1 repetitive sequences. J. Mol. Biol. 246 (3): 401-417. 10.1006/jmbi.1994.0095 7877164
82. Suzuki S. Ono R. Narita T. Pask A.J. Shaw G. Wang C. et al. 2007. Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet. 3 (4): e55. 10.1371/journal.pgen.0030055 17432937 (Pubitemid 46683469)
83. Teichmann M. Seifart K.H. 1995. Physical separation of two different forms of human TFIIIB active in the transcription of the U6 or the VAI gene in vitro. EMBO J. 14 (23): 5974-5983. 8846790
84. Thompson M. Haeusler R.A. Good P.D. Engelke D.R. 2003. Nucleolar clustering of dispersed tRNA genes. Science (Washington, D.C.), 302 (5649): 1399-1401. 10.1126/science.1089814 14631041 (Pubitemid 37452182)
85. Tomilin N.V. 2008. Regulation of mammalian gene expression by retroelements and non-coding tandem repeats. Bioessays, 30 (4): 338-348. 10.1002/bies.20741 18348251 (Pubitemid 351482331)
86. Tsang C.K. Wei Y. Zheng X.F. 2007. Compacting DNA during the interphase: condensin maintains rDNA integrity. Cell Cycle, 6 (18): 2213-2218. 10.4161/cc.6.18.4733 17671437 (Pubitemid 47547695)
87. Umylny B. Presting G. Efird J.T. Klimovitsky B.I. Ward W.S. 2007. Most human Alu and murine B1 repeats are unique. J. Cell. Biochem. 102 (1): 110-121. 10.1002/jcb.21278 17407136 (Pubitemid 47378915)
88. van Zon A. Mossink M.H. Scheper R.J. Sonneveld P. Wiemer E.A. 2003. The vault complex. Cell. Mol. Life Sci. 60 (9): 1828-1837. 10.1007/s00018-003-3030-y 14523546 (Pubitemid 37222581)
89. Walters R.D. Kugel J.F. Goodrich J.A. 2009. InvAluable junk: the cellular impact and function of Alu and B2 RNAs. IUBMB Life, 61 (8): 831-837. 10.1002/iub.227 19621349
90. Weser S. Gruber C. Hafner H.M. Teichmann M. Roeder R.G. Seifart K.H. Meissner W. 2004. Transcription factor (TF)-like nuclear regulator, the 250-kDa form of Homo sapiens TFIIIB", is an essential component of human TFIIIC1 activity. J. Biol. Chem. 279 (26): 27022-27029. 10.1074/jbc.M312790200 15096501 (Pubitemid 38812538)
91. Wheeler B.S. Blau J.A. Willard H.F. Scott K.C. 2009. The impact of local genome sequence on defining heterochromatin domains. PLoS Genet. 5 (4): e1000453. 10.1371/journal.pgen.1000453 19360117
92. Wood A.J. Severson A.F. Meyer B.J. 2010. Condensin and cohesin complexity: the expanding repertoire of functions. Nat. Rev. Genet. 11 (6): 391-404. 10.1038/nrg2794 20442714
93. Xing J. Zhang Y. Han K. Salem A.H. Sen S.K. Huff C.D. et al. 2009. Mobile elements create structural variation: analysis of a complete human genome. Genome Res. 19 (9): 1516-1526. 10.1101/gr.091827.109 19439515
94. Yang Z. Zhu Q. Luo K. Zhou Q. 2001. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature (Lond.), 414 (6861): 317-322. 10.1038/35104575 11713532 (Pubitemid 33097809)
95. Yasuhara J.C. Wakimoto B.T. 2006. Oxymoron no more: the expanding world of heterochromatic genes. Trends Genet. 22 (6): 330-338. 10.1016/j.tig.2006.04. 008 16690158 (Pubitemid 43794921)
96. Yoshinaga S.K. Boulanger P.A. Berk A.J. 1987. Resolution of human transcription factor TFIIIC into two functional components. Proc. Natl. Acad. Sci. U.S.A. 84 (11): 3585-3589. 10.1073/pnas.84.11.3585 3473469 (Pubitemid 17088325)
97. Zhao H. Bourque G. 2009. Recovering genome rearrangements in the mammalian phylogeny. Genome Res. 19 (5): 934-942. 10.1101/gr.086009.108 19411607
98. Zhao X. Pendergrast P.S. Hernandez N. 2001. A positioned nucleosome on the human U6 promoter allows recruitment of SNAPc by the Oct-1 POU domain. Mol. Cell, 7 (3): 539-549. 10.1016/S1097-2765(01)00201-5 11463379 (Pubitemid 32706346)