Modulated contact frequencies at gene-rich loci support a statistical helix model for mammalian chromatin organization

Genome Biology

Volumn 12, Issue 5, 2011, Pages

  Court, Franck ^a   Miro, Julie ^b   Braem, Caroline ^a   Lelay Taha, Marie Noëlle ^a   Brisebarre, Audrey ^a   Atger, Florian ^a   Gostan, Thierry ^a   Weber, Michaël ^a   Cathala, Guy ^a   Forné, Thierry ^a  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^b UNIVERSITÉ DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOINFORMATICS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; GENE CONTROL; GENE INTERACTION; GENE LOCUS; GENETIC CONSERVATION; GENETIC DISTANCE; INTERPHASE; MAMMAL; MATHEMATICAL ANALYSIS; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; STATISTICAL MODEL; ANIMAL; BIOLOGY; CHEMISTRY; CHROMATIN; CHROMOSOME; CHROMOSOME MAP; CONFORMATION; GENETICS; GENOME; GENOMICS; HUMAN; METHODOLOGY; MOLECULAR EVOLUTION; REAL TIME POLYMERASE CHAIN REACTION;

MAMMALIA;

ANIMALS; CHROMATIN; CHROMOSOME MAPPING; CHROMOSOMES; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENETIC LOCI; GENOME; GENOMICS; HUMANS; MAMMALS; MICE; MODELS, STATISTICAL; NUCLEIC ACID CONFORMATION; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 79955725989     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2011-12-5-r42     Document Type: Article

References (37)

1. Cremer T, Cremer M. Chromosome territories. Cold Spring Harb Perspect Biol 2010, 2:a003889. 10.1101/cshperspect.a003889, 2829961, 20300217.
2. Meaburn KJ, Misteli T. Cell biology: chromosome territories. Nature 2007, 445:379-781. 10.1038/445379a, 17251970.
3. Iborra FJ, Pombo A, Jackson DA, Cook PR. Active RNA polymerases are localized within discrete transcription "factories' in human nuclei. J Cell Sci 1996, 109:1427-1436.
4. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293. 10.1126/science.1181369, 2858594, 19815776.
5. Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, Fraser P. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet 2004, 36:1065-1071. 10.1038/ng1423, 15361872.
6. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S, Mitchell JA, Umlauf D, Dimitrova DS, Eskiw CH, Luo Y, Wei CL, Ruan Y, Bieker JJ, Fraser P. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 2010, 42:53-61. 10.1038/ng.496, 20010836.
7. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, de Laat W. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet 2006, 38:1348-1354. 10.1038/ng1896, 17033623.
8. Bantignies F, Grimaud C, Lavrov S, Gabut M, Cavalli G. Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. Genes Dev 2003, 17:2406-2420. 10.1101/gad.269503, 218078, 14522946.
9. Fraser P, Bickmore W. Nuclear organization of the genome and the potential for gene regulation. Nature 2007, 447:413-417. 10.1038/nature05916, 17522674.
10. Naumova N, Dekker J. Integrating one-dimensional and three-dimensional maps of genomes. J Cell Sci 2010, 123:1979-1988. 10.1242/jcs.051631, 20519580.
11. Dekker J, Rippe K, Dekker M, Kleckner N. Capturing chromosome conformation. Science 2002, 295:1306-1311. 10.1126/science.1067799, 11847345.
12. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 2002, 10:1453-1465. 10.1016/S1097-2765(02)00781-5, 12504019.
13. Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL, Honan TA, Rubio ED, Krumm A, Lamb J, Nusbaum C, Green RD, Dekker J. Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res 2006, 16:1299-1309. 10.1101/gr.5571506, 1581439, 16954542.
14. Fraser J, Rousseau M, Shenker S, Ferraiuolo MA, Hayashizaki Y, Blanchette M, Dostie J. Chromatin conformation signatures of cellular differentiation. Genome Biol 2009, 10:R37. 10.1186/gb-2009-10-4-r37, 2688928, 19374771.
15. Horike S, Cai S, Miyano M, Cheng JF, Kohwi-Shigematsu T. Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat Genet 2005, 37:31-40. 10.1038/ng1570, 15608638.
16. Zhao Z, Tavoosidana G, Sjolinder M, Gondor A, Mariano P, Wang S, Kanduri C, Lezcano M, Sandhu KS, Singh U, Pant V, Tiwari V, Kurukuti S, Ohlsson R. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat Genet 2006, 38:1341-1347. 10.1038/ng1891, 17033624.
17. Hagège H, Klous P, Braem C, Splinter E, Dekker J, Cathala G, de Laat W, Forné T. Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2007, 2:1722-1733. 10.1038/nprot.2007.243, 17641637.
18. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, Galjart N, de Laat W. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev 2006, 20:2349-2354. 10.1101/gad.399506, 1560409, 16951251.
19. Braem C, Recolin B, Rancourt RC, Angiolini C, Barthes P, Branchu P, Court F, Cathala G, Ferguson-Smith AC, Forne T. Genomic matrix attachment region and chromosome conformation capture quantitative real time PCR assays identify novel putative regulatory elements at the imprinted Dlk1/Gtl2 locus. J Biol Chem 2008, 283:18612-18620. 10.1074/jbc.M801883200, 18458080.
20. Milligan L, Antoine E, Bisbal C, Weber M, Brunel C, Forné T, Cathala G. H19 gene expression is up-regulated exclusively by stabilization of the RNA during muscle cell differentiation. Oncogene 2000, 19:5810-5816. 10.1038/sj.onc.1203965, 11126368.
21. Milligan L, Forné T, Antoine E, Weber M, Hemonnot B, Dandolo L, Brunel C, Cathala G. Turnover of primary transcripts is a major step in the regulation of mouse H19 gene expression. EMBO Rep 2002, 3:774-779. 10.1093/embo-reports/kvf142, 1084202, 12151337.
22. Gheldof N, Tabuchi TM, Dekker J. The active FMR1 promoter is associated with a large domain of altered chromatin conformation with embedded local histone modifications. Proc Natl Acad Sci USA 2006, 103:12463-12468. 10.1073/pnas.0605343103, 1567902, 16891414.
23. Takada S, Tevendale M, Baker J, Georgiades P, Campbell E, Freeman T, Johnson MH, Paulsen M, Ferguson-Smith AC. Delta-like and Gtl2 are reciprocally expressed, differentially methylated linked imprinted genes on mouse chromosome 12. Curr Biol 2000, 10:1135-1138. 10.1016/S0960-9822(00)00704-1, 10996796.
24. Dekker J. Mapping in vivo chromatin interactions in yeast suggests an extended chromatin fiber with regional variation in compaction. J Biol Chem 2008, 283:34532-34540. 10.1074/jbc.M806479200, 2596406, 18930918.
25. Bono H, Kasukawa T, Hayashizaki Y, Okazaki Y. READ: RIKEN Expression Array Database. Nucleic Acids Res 2002, 30:211-213. 10.1093/nar/30.1.211, 99103, 11752296.
26. Rippe K. Making contacts on a nucleic acid polymer. Trends Biochem Sci 2001, 26:733-740. 10.1016/S0968-0004(01)01978-8, 11738597.
27. Spitz F, Gonzalez F, Duboule D. A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 2003, 113:405-417. 10.1016/S0092-8674(03)00310-6, 12732147.
28. Ringrose L, Chabanis S, Angrand PO, Woodroofe C, Stewart AF. Quantitative comparison of DNA looping in vitro and in vivo: chromatin increases effective DNA flexibility at short distances. EMBO J 1999, 18:6630-6641. 10.1093/emboj/18.23.6630, 1171726, 10581237.
29. Mateos-Langerak J, Bohn M, de Leeuw W, Giromus O, Manders EM, Verschure PJ, Indemans MH, Gierman HJ, Heermann DW, van Driel R, Goetze S. Spatially confined folding of chromatin in the interphase nucleus. Proc Natl Acad Sci USA 2009, 106:3812-3817. 10.1073/pnas.0809501106, 2656162, 19234129.
30. Jhunjhunwala S, van Zelm MC, Peak MM, Murre C. Chromatin architecture and the generation of antigen receptor diversity. Cell 2009, 138:435-448. 10.1016/j.cell.2009.07.016, 2726833, 19665968.
31. Sachs RK, van den Engh G, Trask B, Yokota H, Hearst JE. A random-walk/giant-loop model for interphase chromosomes. Proc Natl Acad Sci USA 1995, 92:2710-2714. 10.1073/pnas.92.7.2710, 42288, 7708711.
32. van den Engh G, Sachs R, Trask BJ. Estimating genomic distance from DNA sequence location in cell nuclei by a random walk model. Science 1992, 257:1410-1412. 10.1126/science.1388286, 1388286.
33. Lutfalla G, Uzé G. Performing quantitative reverse-transcribed polymerase chain reaction experiments. Methods Enzymol 2006, 410:386-400.
34. The R Project for Statistical Computing. , http://www.R-project.org
35. Lercher MJ, Urrutia AO, Hurst LD. Clustering of housekeeping genes provides a unified model of gene order in the human genome. Nat Genet 2002, 31:180-183. 10.1038/ng887, 11992122.
36. De Ferrari L, Aitken S. Mining housekeeping genes with a naive Bayes classifier. BMC Genomics 2006, 7:277. 10.1186/1471-2164-7-277, 1635426, 17074078.
37. Bystricky K, Heun P, Gehlen L, Langowski J, Gasser SM. Long-range compaction and flexibility of interphase chromatin in budding yeast analysed by high-resolution imaging techniques. Proc Natl Acad Sci USA 2004, 101:16495-16500. 10.1073/pnas.0402766101, 534505, 15545610.