Spatial confinement is a major determinant of the folding landscape of human chromosomes

Nucleic Acids Research

Volumn 42, Issue 13, 2014, Pages 8223-8230

  Gürsoy, Gamze ^a   Xu, Yun ^a   Kenter, Amy L ^b   Liang, Jie ^a  

^a University of Illinois at Chicago   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHM; ARTICLE; BIOLOGICAL MODEL; CELL NUCLEUS; CELL SIZE; CHROMATIN; CHROMOSOME ANALYSIS; CHROMOSOME FOLDING; CHROMOSOME STRUCTURE; HUMAN CHROMOSOME; PRIORITY JOURNAL; SPACE;

ALGORITHMS; CELL NUCLEUS SIZE; CHROMATIN; CHROMOSOMES, HUMAN; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION;

EID: 84905587531     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku462     Document Type: Article

References (47)

1. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. and Walter, P. (2002) In:Molecular Biology of the Cell , 4th ed. Garland, New York, pp. 191-234.
2. Fraser, P. and Bickmore, W. (2007) Nuclear organization of the genome and the potential for gene regulation. Nature, 447, 413-417.
3. Lieberman-Aiden, E., van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B.R., Sabo, P.J., Dorschner, M.O. et al. (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science, 326, 289-293.
4. Dostie, J., Richmond, T.A., Arnaout, R.A., Selzer, R.R., Lee, W.L., Honan, T.A., Rubio, E.D., Krumm, A., Lamb, J., Nusbaum, C. et al. (2006) Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res., 16, 1299-1309.
5. Goetze, S., Mateos-Langerak, J., Gierman, H.J., de Leeuw, W., Giromus, O., Indemans, M.H., Koster, J., Ondrej, V., Versteeg, R. and van Driel, R. (2007) The three-dimensional structure of human interphase chromosomes is related to the transcriptome map. Mol. Cell. Biol., 27, 4475-4487.
6. Mateos-Langerak, J., Bohn, M., de Leeuw, W., Giromus, O., Manders, E.M., Verschure, P.J., Indemans, M.H., Gierman, H.J., Heermann, D.W., van Driel, R. et al. (2009) Spatially confined folding of chromatin in the interphase nucleus. Proc. Natl. Acad. Sci. U.S.A., 106, 3812-3817.
7. Zhao, Z., Tavoosidana, G., Sjlinder, M., Gndr, A., Mariano, P., Wang, S., Kanduri, C., Lezcano, M., Sandhu, K.S., Singh, U. et al. (2006) Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat. Genet., 38, 1341-1347.
8. Gavrilov, A., Eivazova, E., Priozhkova, I., Lipinski, M., Razin, S. and Vassetzky, Y. (2009) Chromosome conformation capture (from 3C to 5C) and its ChIP-based modification. Methods Mol. Biol., 567, 171-188.
9. Jhunjhunwala, S., van Zelm, M.C., Peak, M.M., Cutchin, S., Riblet, R., van Dongen, J.J., Grosveld, F.G., Knoch, T.A. and Murre, C. (2008) The 3D structure of the immunoglobulin heavy-chain locus: implications for long-range genomic interactions. Cell, 133, 265-279.
10. Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., Parrinello, H., Tanay, A. and Cavalli, G. (2012) Three-dimensional folding and functional organization principles of the drosophila genome. Cell, 148, 458-472.
11. Cremer, T. and Cremer, C. (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet., 2, 292-301.
12. Barbieri, M., Chotalia, M., Fraser, J., Lavitas, L.M., Dostie, J., Pombo, A. and Nicodemi, M. (2012) Complexity of chromatin folding is captured by the strings and binders switch model. Proc. Natl. Acad. Sci. U.S.A., 109, 16173-16178.
13. Sachs, R.K., van den Engh, G., Trask, B., Yokota, H. and Hearst, J.E. (1995) A random-walk/giant-loop model for interphase chromosomes. Proc. Natl. Acad. Sci. U.S.A., 92, 2710-2714.
14. Bohn, M., Heermann, D.W. and van Driel, R. (2007) Random loop model for long polymers. Phys. Rev. E, 76, 051805.
15. Tark-Dame, M., van Driel, R. and Heermann, D.W. (2011) Chromatin folding-from biology to polymer models and back. J. Cell Sci., 124, 839-845.
16. Mirny, L.A. (2011) The fractal globule as a model of chromatin architecture in the cell. Chromosome Res., 19, 37-51.
17. Bohn, M. and Heermann, D.W. (2010) Diffusion-driven looping provides a consistent framework for chromatin organization. PloS One, 5, e12218.
18. Kalhor, R., Tjong, H., Jayathilaka, N., Alber, F. and Chen, L. (2012) Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol., 30, 90-98.
19. Hahnfeldt, P., Hearst, J.E., Brenner, D.J., Sachs, R.K. and Hlatky, L.R. (1993) Polymer models for interphase chromosomes. Proc. Natl. Acad. Sci. U.S.A., 90, 7854-7858.
20. Heermann, D.W., Jerabek, H., Liu, L. and Li, Y. (2012) A model for the 3D chromatin architecture of pro and eukaryotes. Methods, 58, 307-314.
21. Iyer, B. and Arya, G. (2012) Lattice animal model of chromosome organization. Phys. Rev. E, 86, 011911.
22. Tjong, H., Gong, K., Chen, L. and Alber, F. (2012) Physical tethering and volume exclusion determine higher-order genome organization in budding yeast. Genome Res., 22, 1295-1305.
23. Liu, J.S. and Chen, R. (1998) Sequential monte carlo methods for dynamic systems. J. Am. Stat. Assoc., 93, 1032-1044.
24. Zhang, J., Chen, R., Tang, C. and Liang, J. (2003) Origin of scaling behavior of protein packing density: a sequential monte carlo study of compact long chain polymers. J. Chem. Phys., 118, 6102.
25. Lin, M., Zhang, J., Lu, H.M., Chen, R. and Liang, J. (2011) Constrained proper sampling of conformations of transition state ensemble of protein folding. J. Chem. Phys., 134, 075103.
26. Finch, J.T. and Klug, A. (1976) Solenoidal model for superstructure in chromatin. Proc. Natl. Acad. Sci. U.S.A., 73, 1897-1901.
27. Bystricky, K., Heun, P., Gehlen, L., Langowski, J. and Gasser, S.M. (2004) Long-range compaction and flexibility of interphase chromatin in budding yeast analyzed by high-resolution imaging techniques. Proc. Natl. Acad. Sci. U.S.A., 101, 16495-16500.
28. Gerchman, S.E. and Ramakrishnan, V. (1987) Chromatin higher-order structure studied by neutron scattering and scanning transmission electron microscopy. Proc. Natl. Acad. Sci. U.S.A., 84, 7802-7806.
29. Wedemann, G. and Langowski, J. (2002) Computer simulation of the 30-nanometer chromatin fiber. Biophys. J., 82, 2847-2859.
30. Liang, J., Zhang, J. and Chen, R. (2002) Statistical geometry of packing defects of lattice chain polymer from enumeration and sequential Monte Carlo method. J. Chem. Phys., 117, 3511-3521.
31. Lin, M., Lu, H.M., Chen, R. and Liang, J. (2008) Generating properly weighted ensemble of conformations of proteins from sparse or indirect distance constraints. J. Chem. Phys., 129, 094101.
32. Lin, M., Chen, R. and Liang, J. (2008) Statistical geometry of lattice chain polymers with voids of defined shapes: sampling with strong constraints. J. Chem. Phys., 128, 084903.
33. Zhang, J., Dundas, J., Lin, M., Chen, R., Wang, W. and Liang, J. (2009) Prediction of geometrically feasible three dimensional structures of pseudoknotted RNA through free energy estimation. RNA, 15, 2248-2263
34. de Gennnes, P.G. (1979) In: Scaling Concepts in Polymer Physics. Cornell University Press, New York, pp. 1-100.
35. Cook, P.R. (1999) The organization of replication and transcription. Science, 284, 1790-1795.
36. Kreth, G., Finsterle, J., von Hase, J., Cremer, M. and Cremer, C. (2004) Radial arrangement of chromosome territories in human cell nuclei: a computer model approach based on gene density indicates a probabilistic global positioning code. Biophys. J., 86, 2803-2812.
37. Dixon, J.R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J.S. and Ren, B. (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature, 485, 376-380.
38. Nora, E.P., Lajoie, B.R., Schulz, E.G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., van Berkum, N.L., Meisig, J., Sedat, J. et al. (2012) Spatial partitioning of the regulatory landscape of the x-inactivation centre. Nature, 485, 381-385.
39. Cremer, T., Kreth, G., Koester, H., Fink, R.H., Heintzmann, R., Cremer, M., Solovei, I., Zink, D. and Cremer, C. (2000) Chromosome territories, interchromatin domain compartment, and nuclear matrix: an integrated view of the functional nuclear architecture. Crit. Rev. Eukaryot. Gene Expr., 10, 179-212.
40. Renda, M., Baglivo, I., Burgess-Beusse, B., Esposito, S., Fattorusso, R., Felsenfeld, G. and Pedone, P.V. (2007) Critical DNA binding interactions of the insulator protein CTCF: a small number of zinc fingers mediate strong binding, and a single finger-DNA interaction controls binding at imprinted loci. J. Biol. Chem., 282, 33336-33345.
41. Zwaka, T.P. and Thomson, J.A. (2003) Homologous recombination in human embryonic stem cells. Nat. Biotechnol., 21, 319-321.
42. Dahl, K.N., Ribeiro, A.J.S. and Lammerding, J. (2008) Nuclear shape, mechanics, and mechanotransduction. Circ. Res., 102, 1307-1318.
43. Pajerowski, J.D., Dahl, K.N., Zhong, F.L., Sammak, P.J. and Discher, D.E. (2007) Physical plasticity of the nucleus in stem cell differentiation. Proc. Natl. Acad. Sci. U.S.A., 104, 15619-15624.
44. Krivega, I. and Dean, A. (2012) Enhancer and promoter interactions-long distance calls. Curr. Opin. Genet. Dev., 22, 79-85.
45. Ong, C.T. and Corces, V.G. (2011) Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat. Rev. Genet., 12, 283-293.
46. Sexton, T., Bantignies, F. and Cavalli, G. (2009) Genomic interactions: chromatin loops and gene meeting points in transcriptional regulation. Semin. Cell Dev. Biol., 20, 849-855.
47. Fussner, E., Strauss, M., Djuric, U., Li, R., Ahmed, K., Hart, M., Ellis, J. and Bazett-Jones, D.P. (2012) Open and closed domains in the mouse genome are configured as 10-nm chromatin fibres. EMBO Rep., 13, 992-996.