Understanding the regulatory and transcriptional complexity of the genome through structure

Genome Research

Volumn 23, Issue 7, 2013, Pages 1081-1088

  Mercer, Tim R ^a   Mattick, John S ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CALCIUM; COHESIN; CONNECTIN; DNA; DNA DIRECTED RNA POLYMERASE; FORMALDEHYDE; HISTONE; KINESIN; LAMIN; MULTIPROTEIN COMPLEX; MYOSIN; RESTRICTION ENDONUCLEASE; RNA POLYMERASE II; STAT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UNTRANSLATED RNA;

CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CHROMOSOME; CHROMOSOME STRUCTURE; DEVELOPMENT; FIBROBLAST; GENE EXPRESSION; GENE STRUCTURE; GENETIC TRANSCRIPTION; GENOME; HUMAN; HUMAN GENOME; LABORATORY; LANDSCAPE; MICROSCOPY; MOUSE; NATURAL SCIENCE; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; RNA SPLICING; TRANSCRIPTION REGULATION;

ANIMALS; CELL NUCLEUS; CHROMATIN; GENE EXPRESSION REGULATION; GENOME; GENOMIC IMPRINTING; HUMANS; NUCLEAR MATRIX; RNA FOLDING; TRANSCRIPTION, GENETIC;

EID: 84880060145     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.156612.113     Document Type: Review

References (102)

1. Asbury TM, Mitman M, Tang J, Zheng WJ. 2010. Genome3D: A viewermodel framework for integrating and visualizing multi-scale epigenomic information within a three-dimensional genome. BMC Bioinformatics 11: 444.
2. Bancaud A, Lavelle C, Huet S, Ellenberg J. 2012. A fractal model for nuclear organization: Current evidence and biological implications. Nucleic Acids Res 40: 8783-8792.
3. Bartova E, Krejci J, Harnicarova A, Galiova G, Kozubek S. 2008. Histone modifications and nuclear architecture: A review. J Histochem Cytochem 56: 711-721.
4. Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K, Fauth C, Muller S, Eils R, Cremer C, Speicher MR, et al. 2005. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol 3: e157.
5. Boutanaev AM, Kalmykova AI, Shevelyov YY, Nurminsky DI. 2002. Large clusters of co-expressed genes in the Drosophila genome. Nature 420: 666-669.
6. Boyle S, Rodesch MJ, Halvensleben HA, Jeddeloh JA, Bickmore WA. 2011. Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis. Chromosome Res 19: 901-909.
7. Caron H, van Schaik B, van der MeeM, Baas F, Riggins G, van Sluis P, Hermus MC, van Asperen R, Boon K, Voute PA, et al. 2001. The human transcriptome map: Clustering of highly expressed genes in chromosomal domains. Science 291: 1289-1292.
8. Cawley S, Bekiranov S, Ng HH, Kapranov P, Sekinger EA, Kampa D, Piccolboni A, Sementchenko V, Cheng J, Williams AJ, et al. 2004. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 116: 499-509.
9. Chepelev I, Wei G, Wangsa D, Tang Q, Zhao K. 2012. Characterization of genome-wide enhancer-promoter interactions reveals co-expression of interacting genes and modes of higher order chromatin organization. Cell Res 22: 490-503.
10. Cheutin T, Cavalli G. 2012. Progressive polycomb assembly on H3K27me3 compartments generates polycomb bodies with developmentally regulated motion. PLoS Genet 8: e1002465.
11. Chuang CH, Carpenter AE, Fuchsova B, Johnson T, de Lanerolle P, Belmont AS. 2006. Long-range directional movement of an interphase chromosome site. Curr Biol 16: 825-831.
12. Clemson CM, Hutchinson JN, Sara SA, Ensminger AW, Fox AH, Chess A, Lawrence JB. 2009. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell 33: 717-726.
13. Cook PR. 2010. A model for all genomes: The role of transcription factories. J Mol Biol 395: 1-10.
14. de Lanerolle P, Serebryannyy L. 2011. Nuclear actin and myosins: Life without filaments. Nat Cell Biol 13: 1282-1288.
15. deWit E, de LaatW. 2012. A decade of 3C technologies: Insights into nuclear organization. Genes Dev 26: 11-24.
16. Dekker J, Rippe K, Dekker M, Kleckner N. 2002. Capturing chromosome conformation. Science 295: 1306-1311.
17. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485: 376-380.
18. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, LinW, Schlesinger F, et al. 2012. Landscape of transcription in human cells. Nature 489: 101-108.
19. Dundr M, Ospina JK, Sung MH, John S, Upender M, Ried T, Hager GL, Matera AG. 2007. Actin-dependent intranuclear repositioning of an active gene locus in vivo. J Cell Biol 179: 1095-1103.
20. Ebralidze AK, Guibal FC, Steidl U, Zhang P, Lee S, Bartholdy B, Jorda MA, Petkova V, Rosenbauer F, Huang G, et al. 2008. PU.1 expression is modulated by the balance of functional sense and antisense RNAs regulated by a shared cis-regulatory element. Genes Dev 22: 2085-2092.
21. Edelman LB, Fraser P. 2012. Transcription factories: Genetic programming in three dimensions. Curr Opin Genet Dev 22: 110-114.
22. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
23. Eskiw CH, Rapp A, Carter DR, Cook PR. 2008. RNA polymerase II activity is located on the surface of protein-rich transcription factories. J Cell Sci 121: 1999-2007.
24. The FANTOM Consortium. 2005. The transcriptional landscape of the mammalian genome. Science 309: 1559-1563.
25. Ferrai C, Naum-Ongania G, Longobardi E, Palazzolo M, Disanza A, Diaz VM, CrippaMP, Scita G, Blasi F. 2009. Induction of HoxB transcription by retinoic acid requires actin polymerization.Mol Biol Cell 20: 3543-3551.
26. Fisher WW, Li JJ, Hammonds AS, Brown JB, Pfeiffer BD, Weiszmann R, MacArthur S, Thomas S, Stamatoyannopoulos JA, Eisen MB, et al. 2012. DNA regions bound at low occupancy by transcription factors do not drive patterned reporter gene expression in Drosophila. Proc Natl Acad Sci 109: 21330-21335.
27. Fomproix N, Percipalle P. 2004. An actin-myosin complex on actively transcribing genes. Exp Cell Res 294: 140-148.
28. 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.
29. Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH, et al. 2009. An oestrogen-receptor-a-bound human chromatin interactome. Nature 462: 58-64.
30. Gerstein MB, Bruce C, Rozowsky JS, Zheng D, Du J, Korbel JO, Emanuelsson O, Zhang ZD, Weissman S, Snyder M. 2007. What is a gene, post-ENCODE? History and updated definition. Genome Res 17: 669-681.
31. Gingeras TR. 2007.Origin of phenotypes: Genes and transcripts. Genome Res 17: 682-690.
32. Hakim O, Sung MH, Voss TC, Splinter E, John S, Sabo PJ, Thurman RE, Stamatoyannopoulos JA, de Laat W, Hager GL. 2011. Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res 21: 697-706.
33. Hakim O, Sung MH, Nakayamada S, Voss TC, Baek S, Hager GL. 2013. Spatial congregation of STAT binding directs selective nuclear architecture during T-cell functional differentiation. Genome Res 23: 462-472.
34. Hernandez-Verdun D, Roussel P, Thiry M, Sirri V, Lafontaine DL. 2010. The nucleolus: Structure/function relationship in RNA metabolism. Wiley Interdiscip Rev RNA 1: 415-431.
35. Hofmann WA, Stojiljkovic L, Fuchsova B, Vargas GM, Mavrommatis E, Philimonenko V, Kysela K, Goodrich JA, Lessard JL, Hope TJ, et al. 2004. Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II. Nat Cell Biol 6: 1094-1101.
36. International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.
37. Jackson DA, Hassan AB, Errington RJ, Cook PR. 1993. Visualization of focal sites of transcription within human nuclei. EMBO J 12: 1059-1065.
38. Kalhor R, Tjong H, Jayathilaka N, Alber F, Chen L. 2012. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat Biotechnol 30: 90-98.
39. Kapranov P, Drenkow J, Cheng J, Long J, Helt G, Dike S, Gingeras TR. 2005. Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays. Genome Res 15: 987-997.
40. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R,Willingham AT, Stadler PF, Hertel J, Hackermuller J, Hofacker IL, et al. 2007a. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316: 1484-1488.
41. Kapranov P, Willingham AT, Gingeras TR. 2007b. Genome-wide transcription and the implications for genomic organization. Nat Rev Genet 8: 413-423.
42. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. 2010. Widespread transcription at neuronal activity-regulated enhancers. Nature 465: 182-187.
43. Kornblihtt AR, Schor IE, Allo M, Dujardin G, Petrillo E, Munoz MJ. 2013. Alternative splicing: A pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol 14: 153-165.
44. Lan X,Witt H, Katsumura K, Ye Z,WangQ, Bresnick EH, Farnham PJ, Jin VX. 2012. Integration of Hi-C and ChIP-seq data reveals distinct types of chromatin linkages. Nucleic Acids Res 40: 7690-7704.
45. Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, Batzoglou S, Bernstein BE, Bickel P, Brown JB, Cayting P, et al. 2012. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 22: 1813-1831.
46. Lee BK, Iyer VR. 2012. Genome-wide studies of CCCTC-binding factor (CTCF) and cohesin provide insight into chromatin structure and regulation. J Biol Chem 287: 30906-30913.
47. Lemons D, McGinnis W. 2006. Genomic evolution of Hox gene clusters. Science 313: 1918-1922.
48. Lercher MJ, Urrutia AO, Hurst LD. 2002. Clustering of housekeeping genes provides a unified model of gene order in the human genome. Nat Genet 31: 180-183.
49. Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M,Wang P, Poh HM, Goh Y, Lim J, Zhang J, et al. 2012. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148: 84-98.
50. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326: 289-293.
51. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T. 2011. Epigenetics in alternative pre-mRNA splicing. Cell 144: 16-26.
52. Mallo M,Wellik DM, Deschamps J. 2010. Hox genes and regional patterning of the vertebrate body plan. Dev Biol 344: 7-15.
53. Mao YS, Zhang B, Spector DL. 2011. Biogenesis and function of nuclear bodies. Trends Genet 27: 295-306.
54. Marti-Renom MA, Mirny LA. 2011. Bridging the resolution gap in structural modeling of 3D genome organization. PLoS Comput Biol 7: e1002125.
55. Mattick JS. 2003. Challenging the dogma: The hidden layer of non-proteincoding RNAs in complex organisms. BioEssays 25: 930-939.
56. Mehta IS, Amira M, Harvey AJ, Bridger JM. 2010. Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Genome Biol 11: R5.
57. Melnik S, Deng B, Papantonis A, Baboo S, Carr IM, Cook PR. 2011. The proteomes of transcription factories containing RNA polymerases I, II or III. Nat Methods 8: 963-968.
58. Melo CA, Drost J,Wijchers PJ, van deWerken H, deWit E, Vrielink JA, Elkon R, Melo SA, Leveille N, Kalluri R, et al. 2012. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol Cell 49: 524-525.
59. Mercer TR, Dinger ME, Mattick JS. 2009. Long non-coding RNAs: Insights into functions. Nat Rev Genet 10: 155-159.
60. Mercer TR, Gerhardt DJ, Dinger ME, Crawford J, Trapnell C, Jeddeloh JA, Mattick JS, Rinn JL. 2012. Targeted RNA sequencing reveals the deep complexity of the human transcriptome. Nat Biotechnol 30: 99-104.
61. Moabbi AM, Agarwal N, El Kaderi B, Ansari A. 2012. Role for gene looping in intron-mediated enhancement of transcription. Proc Natl Acad Sci 109: 8505-8510.
62. Mondal T, Rasmussen M, Pandey GK, Isaksson A, Kanduri C. 2010. Characterization of the RNA content of chromatin. Genome Res 20: 899-907.
63. Moore MJ, Proudfoot NJ. 2009. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136: 688-700.
64. Moorman C, Sun LV, Wang J, de Wit E, Talhout W, Ward LD, Greil F, Lu XJ, White KP, Bussemaker HJ, et al. 2006. Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster. Proc Natl Acad Sci 103: 12027-12032.
65. Morey C, Kress C, Bickmore WA. 2009. Lack of bystander activation shows that localization exterior to chromosome territories is not sufficient to up-regulate gene expression. Genome Res 19: 1184-1194.
66. Nemeth A, Langst G. 2011. Genome organization in and around the nucleolus. Trends Genet 27: 149-156.
67. Neph S, Vierstra J, Stergachis AB, Reynolds AP, Haugen E, Vernot B, Thurman RE, John S, Sandstrom R, Johnson AK, et al. 2012. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 489: 83-90.
68. Noordermeer D, Leleu M, Splinter E, Rougemont J, De LaatW, Duboule D. 2011. The dynamic architecture ofHox gene clusters. Science 334: 222-225.
69. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, et al. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485: 381-385.
70. O'Reilly D, Greaves DR. 2007. Cell-type-specific expression of the human CD68 gene is associated with changes in Pol II phosphorylation and short-range intrachromosomal gene looping. Genomics 90: 407-415.
71. O'Sullivan JM, Tan-Wong SM, Morillon A, Lee B, Coles J, Mellor J, Proudfoot NJ. 2004. Gene loops juxtapose promoters and terminators in yeast. Nat Genet 36: 1014-1018.
72. Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, et al. 2004. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 36: 1065-1071.
73. Osborne CS, Chakalova L, Mitchell JA, Horton A, Wood AL, Bolland DJ, Corcoran AE, Fraser P. 2007. Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol 5: e192.
74. Papantonis A, Cook PR. 2011. Fixing the model for transcription: The DNA moves, not the polymerase. Transcription 2: 41-44.
75. Papantonis A, Larkin JD,Wada Y, Ohta Y, Ihara S, Kodama T, Cook PR. 2010. Active RNA polymerases: Mobile orimmobile molecular machines? PLoS Biol 8: e1000419.
76. Pestic-Dragovich L, Stojiljkovic L, Philimonenko AA, Nowak G, Ke Y, Settlage RE, Shabanowitz J, Hunt DF, Hozak P, de Lanerolle P. 2000. A myosin I isoform in the nucleus. Science 290: 337-341.
77. Philimonenko VV, Zhao J, Iben S, Dingova H, Kysela K, Kahle M, Zentgraf H, Hofmann WA, de Lanerolle P, Hozak P, et al. 2004. Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat Cell Biol 6: 1165-1172.
78. Pranchevicius MC, Baqui MM, Ishikawa-Ankerhold HC, Lourenco EV, Leao RM, Banzi SR, dos Santos CT, Roque-Barreira MC, Espreafico EM, Larson RE. 2008. Myosin Va phosphorylated on Ser1650 is found in nuclear speckles and redistributes to nucleoli upon inhibition of transcription. Cell Motil Cytoskeleton 65: 441-456.
79. Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, Eaton ML, Landolin JM, Bristow CA, Ma L, Lin MF, et al. 2010. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330: 1787-1797.
80. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S, Mitchell JA, Umlauf D, Dimitrova DS, et al. 2010. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 42: 53-61.
81. Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, Hoichman M, Parrinello H, Tanay A, Cavalli G. 2012. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148: 458-472.
82. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S,Wagner U, Dixon J, Lee L, Lobanenkov VV, et al. 2012. A map of the cis-regulatory sequences in the mouse genome. Nature 488: 116-120.
83. Shevtsov SP, Dundr M. 2011. Nucleation of nuclear bodies by RNA. Nat Cell Biol 13: 167-173.
84. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S. 2011. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479: 74-79.
85. Simon DN, Wilson KL. 2011. The nucleoskeleton as a genome-associated dynamic 'network of networks'. Nat Rev Mol Cell Biol 12: 695-708.
86. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, de LaatW. 2006. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation captureon-chip (4C). Nat Genet 38: 1348-1354.
87. Singh BN, Hampsey M. 2007. A transcription-independent role for TFIIB in gene looping. Mol Cell 27: 806-816.
88. Spellman PT, Rubin GM. 2002. Evidence for large domains of similarly expressed genes in the Drosophila genome. J Biol 1: 5.
89. Strickfaden H, Zunhammer A, van Koningsbruggen S, Kohler D, Cremer T. 2010. 4D chromatin dynamics in cycling cells: Theodor Boveri's hypotheses revisited. Nucleus 1: 284-297.
90. Tan-Wong SM, French JD, Proudfoot NJ, Brown MA. 2008. Dynamic interactions between the promoter and terminator regions of the mammalian BRCA1 gene. Proc Natl Acad Sci 105: 5160-5165.
91. Tan-Wong SM, Zaugg JB, Camblong J, Xu Z, Zhang DW, Mischo HE, Ansari AZ, Luscombe NM, Steinmetz LM, Proudfoot NJ. 2012. Gene loops enhance transcriptional directionality. Science 338: 671-675.
92. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, et al. 2012. The accessible chromatin landscape of the human genome. Nature 489: 75-82.
93. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W. 2002. Looping and interaction between hypersensitive sites in the active b-globin locus. Mol Cell 10: 1453-1465.
94. Towbin BD, Gonzalez-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.
95. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q,Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA, et al. 2010. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39: 925-938.
96. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, et al. 2001. The sequence of the human genome. Science 291: 1304-1351.
97. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, et al. 2011. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472: 120-124.
98. Wansink DG, Schul W, van der Kraan I, van Steensel B, van Driel R, de Jong L. 1993. Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J Cell Biol 122: 283-293.
99. Xu M, Cook PR. 2008. Similar active genes cluster in specialized transcription factories. J Cell Biol 181: 615-623.
100. Yang L, Lin C, Liu W, Zhang J, Ohgi KA, Grinstein JD, Dorrestein PC, Rosenfeld MG. 2011. ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 147: 773-788.
101. Yao J, Ardehali MB, Fecko CJ, Webb WW, Lis JT. 2007. Intranuclear distribution and local dynamics of RNA polymerase II during transcription activation. Mol Cell 28: 978-990.
102. Zhou GL, Xin L, Song W, Di LJ, Liu G, Wu XS, Liu DP, Liang CC. 2006. Active chromatin hub of the mouse a-globin locus forms in a transcription factory of clustered housekeeping genes. Mol Cell Biol 26: 5096-5105.