Segmental folding of chromosomes: A basis for structural and regulatory chromosomal neighborhoods?

Abstract

We discuss here a series of testable hypotheses concerning the role of chromosome folding into topologically associating domains (TADs). Several lines of evidence suggest that segmental packaging of chromosomal neighborhoods may underlie features of chromatin that span large domains, such as heterochromatin blocks, association with the nuclear lamina and replication timing. By defining which DNA elements preferentially contact each other, the segmentation of chromosomes into TADs may also underlie many properties of long‐range transcriptional regulation. Several observations suggest that TADs can indeed provide a structural basis to regulatory landscapes, by controlling enhancer sharing and allocation. We also discuss how TADs may shape the evolution of chromosomes, by causing maintenance of synteny over large chromosomal segments. Finally we suggest a series of experiments to challenge these ideas and provide concrete examples illustrating how they could be practically applied.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 72

1. 1.

   Dekker J, Klecker N. Capturing chromosome conformation. Science. 2002;295:1306-11.

   Not in our library10.1126/science.1067799

2. 2.

   De Wit E, de Laat W. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 2012;26:11-24.

   Not in our library10.1101/gad.179804.111

3. 3.

   Tolhuis B, Palstra RJ, Splinter E, Grosveld F, et al. Looping and interaction between hypersensitive sites in the active [beta]-globin locus. Mol Cell. 2002;10:1453-65.

   Not in our library10.1016/s1097-2765(02)00781-5

4. 4.

   Simonis M, Klous P, Splinter E, Moshkin Y, et al. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture–on-chip (4C). Nat Genet. 2006;38:1348-54.

   Not in our library10.1038/ng1896

5. 5.

   Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326:289-93.

   Not in our library10.1126/science.1181369

6. 6.

   Hakim O, Sung M-H, Nakayamada S, Voss T, et al. Spatial congregation of STAT binding directs selective nuclear architecture during T cell functional differentiation. Genome Res. 2013;23:462-72.

   Not in our library10.1101/gr.147652.112

7. 7.

   Kalhor R, Tjong H, Jayathilaka N, Alber F, et al. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat Biotechnol. 2012;30:90-8.

   Not in our library10.1038/nbt.2057

8. 8.

   Li G, Ruan X, Auerbach RK, Sandhu KS, et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell. 2012;148:84-98.

   Not in our library10.1016/j.cell.2011.12.014

9. 9.

   Schoenfelder S, Sexton T, Chakalova L, Cope NF, et al. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet. 2010;42:53-61.

   Not in our library10.1038/ng.496

10. 10.

    Yaffe E, Tanay A. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat Genet. 2011;43:1059-65.

    Not in our library10.1038/ng.947

11. 11.

    Dostie J, Richmond TA, Arnaout RA, Selzer RR, et al. Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 2006;16:1299-309.

    Not in our library10.1101/gr.5571506

12. 12.

    Dixon JR, Selvaraj S, Yue F, Kim A, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485:376-80.

    Not in our library10.1038/nature11082

13. 13.

    Nora EP, Lajoie BR, Schulz EG, Giorgetti L, et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature. 2012;485:381-5.

    Not in our library10.1038/nature11049

14. 14.

    Hou C, Li L, Qin ZS, Corces VG. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol Cell. 2012;48:471-84.

    Not in our library10.1016/j.molcel.2012.08.031

15. 15.

    Sexton T, Yaffe E, Kenigsberg E, Bantignies F, et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell. 2012;148:458-72.

    Not in our library10.1016/j.cell.2012.01.010

16. 16.

    De Graaf CA, van Steensel B. Chromatin organization: form to function. Curr Opin Genet Dev. 2013;23:185-90.

    Not in our library10.1016/j.gde.2012.11.011

17. 17.

    Tanay A, Cavalli G. Chromosomal domains: epigenetic contexts and functional implications of genomic compartmentalization. Curr Opin Genet Dev. 2013;23:197-203.

    Not in our library10.1016/j.gde.2012.12.009

18. 18.

    Markaki Y, Gunkel M, Schermelleh L, Beichmanis S, et al. Functional nuclear organization of transcription and DNA replication: a topographical marriage between chromatin domains and the interchromatin compartment. Cold Spring Harb Symp Quant Biol. 2010;75:475-92.

    Not in our library10.1101/sqb.2010.75.042

19. 19.

    White R. Packaging the fly genome: domains and dynamics. Brief Funct Genom. 2012;11:347-55.

    Not in our library10.1093/bfgp/els020

20. 20.

    Tanizawa H, Iwasaki O, Tanaka A, Capizzi JR, et al. Mapping of long-range associations throughout the fission yeast genome reveals global genome organization linked to transcriptional regulation. Nucleic Acids Res. 2010;38:8164-77.

    Not in our library10.1093/nar/gkq955

21. 21.

    Duan Z, Andronescu M, Schutz K, McIlwain S, et al. A three-dimensional model of the yeast genome. Nature. 2010;465:363-7.

    Not in our library10.1038/nature08973

22. 22.

    Bickmore WA, van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell. 2013;152:1270-84.

    Not in our library10.1016/j.cell.2013.02.001

23. 23.

    De Wit E, van Steensel B. Chromatin domains in higher eukaryotes: insights from genome-wide mapping studies. Chromosoma. 2008;118:25-36.

    Not in our library10.1007/s00412-008-0186-0

24. 24.

    Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell. 2010;143:212-24.

    Not in our library10.1016/j.cell.2010.09.009

25. 25.

    Van Steensel B. Chromatin: constructing the big picture. EMBO J. 2011;30:1885-95.

    Not in our library10.1038/emboj.2011.135

26. 26.

    Hu S, Cheng L, Wen B. Large chromatin domains in pluripotent and differentiated cells. Acta Biochim Biophys Sin. 2012;44:48-53.

    Not in our library10.1093/abbs/gmr108

27. 27.

    Pauler FM, Sloane MA, Huang R, Regha K, et al. H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res. 2009;19:221-33.

    Not in our library10.1101/gr.080861.108

28. 28.

    Wen B, Wu H, Shinkai Y, Irizarry RA, et al. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet. 2009;41:246-50.

    Not in our library10.1038/ng.297

29. 29.

    Hawkins RD, Hon GC, Lee LK, Ngo Q, et al. Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell. 2010;6:479-91.

    Not in our library10.1016/j.stem.2010.03.018

30. 30.
    PcG Proteins, DNA Methylation, and Gene Repression by Chromatin Looping · 2008

    No notice
31. 31.

    Towbin BD, González-Aguilera C, Sack R, Gaidatzis D, et al. Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell. 2012;150:934-47.

    Not in our library10.1016/j.cell.2012.06.051

32. 32.

    Iacovoni JS, Caron P, Lassadi I, Nicolas E, et al. High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. EMBO J. 2010;29:1446-57.

    Not in our library10.1038/emboj.2010.38

33. 33.

    Dodd IB, Micheelsen MA, Sneppen K, Thon G. Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell. 2007;129:813-22.

    Not in our library10.1016/j.cell.2007.02.053

34. 34.

    Hon GC, Hawkins RD, Caballero OL, Lo C, et al. Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer. Genome Res. 2012;22:246-58.

    Not in our library10.1101/gr.125872.111

35. 35.

    Guelen L, Pagie L, Brasset E, Meuleman W, et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature. 2008;453:948-51.

    Not in our library10.1038/nature06947

36. 36.

    Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SWM, et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell. 2010;38:603-13.

    Not in our library10.1016/j.molcel.2010.03.016

37. 37.

    Stransky N, Vallot C, Reyal F, Bernard-Pierrot I, et al. Regional copy number–independent deregulation of transcription in cancer. Nat Genet. 2006;38:1386-96.

    Not in our library10.1038/ng1923

38. 38.

    Vallot C, Stransky N, Bernard-Pierrot I, Hérault A, et al. A novel epigenetic phenotype associated with the most aggressive pathway of bladder tumor progression. J Natl Cancer Inst. 2011;103:47-60.

    Not in our library10.1093/jnci/djq470

39. 39.
    Global Reorganization of Replication Domains During Embryonic Stem Cell Differentiation · 2008

    No notice
40. 40.

    Ryba T, Hiratani I, Lu J, Itoh M, et al. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 2010;20:761-70.

    Not in our library10.1101/gr.099655.109

Cited by papers we hold 8

• Evolutionary stability of topologically associating domains is associated with conserved gene regulation · 2018
  No notice
• Analysis methods for studying the 3D architecture of the genome · 2015
  No notice
• Chromatin interaction analysis reveals changes in small chromosome and telomere clustering between epithelial and breast cancer cells · 2015
  No notice
• HiCPlotter integrates genomic data with interaction matrices · 2015
  No notice
• Spatial genome organization: contrasting views from chromosome conformation capture and fluorescence in situ hybridization · 2014
  No notice
• Chromatin as dynamic 10-nm fibers · 2014
  No notice
• Temporal dynamics and developmental memory of 3D chromatin architecture at Hox gene loci · 2014
  No notice
• Clustering of Tissue-Specific Sub-TADs Accompanies the Regulation of HoxA Genes in Developing Limbs · 2013
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.