Stacked thin layers of metaphase chromatin explain the geometry of chromosome rearrangements and banding

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Daban, Joan Ramon ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN; DNA;

CHEMISTRY; CHROMATID; CHROMATIN; CHROMOSOME BANDING PATTERN; CYTOLOGY; FEMALE; GENE TRANSLOCATION; GENETICS; HUMAN; KARYOTYPING; METAPHASE; ONION; OVARY TUMOR; PATHOLOGY; ULTRASTRUCTURE;

CHROMATIDS; CHROMATIN; CHROMOSOME BANDING; DNA; FEMALE; HUMANS; KARYOTYPING; METAPHASE; ONIONS; OVARIAN NEOPLASMS; TRANSLOCATION, GENETIC;

EID: 84943632019     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14891     Document Type: Article

References (62)

1. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. and Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260 (1997).
2. Daban, J. R. Electron microscopy and atomic force microscopy studies of chromatin and metaphase chromosome structure. Micron 42, 733-750 (2011).
3. Luger, K., Dechassa, M. L. and Tremethick, D. J. New insight into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat. Rev. Mol. Cell. Biol. 13, 436-447 (2012).
4. Rippe, K. The folding of nucleosome chains in Genome organization and function in the cell nucleus (ed. Rippe, K.) 139-167 (Wiley-VCH, 2012).
5. Collepardo-Guevara, R. and Schlick, T. Chromatin fiber polymorphism triggered by variations of DNA linker length. Proc. Natl. Acad. Sci. USA 111, 8061-8066 (2014).
6. Boule, J. B., Mozziconacci, J. and Lavelle, C. The polymorphisms of the chromatin fiber. J. Phys. Condens. Matter 27, 033101 (2015).
7. Daban, J. R. High concentration of DNA in condensed chromatin. Biochem. Cell Biol. 81, 91-99 (2003).
8. Daban, J. R. The energy components of stacked chromatin layers explain the morphology, dimensions and mechanical properties of metaphase chromosomes. J. R. Soc. Interface 11, 20131043 (2014).
9. International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).
10. Paulson, J. R. and Laemmli, U. K. The structure of histone-depleted metaphase chromosomes. Cell 12, 817-828 (1977).
11. Rattner, J. B. and Lin, C. C. Radial loops and helical coils coexist in metaphase chromosomes. Cell 42, 291-296 (1985).
12. Strukov, Y. G., Wang, Y. and Belmont, A. S. Engineered chromosome regions with altered sequence composition demonstrate hierarchical large-scale folding within metaphase chromosomes. J. Cell Biol. 162, 23-35 (2003).
13. Kireeva, N., Lakonishok, M., Kireev, I., Hirano, T. and Belmont, A. S. Visualization of early chromosome condensation: a hierarchical folding, axial glue model of chromosome structure. J. Cell Biol. 166, 775-785 (2004).
14. Poirier, M. G. and Marko, J. F. Mitotic chromosomes are chromatin networks without a mechanically contiguous protein scaffold. Proc. Natl. Acad Sci. USA 99, 15393-15397 (2002).
15. Eltsov, M., MacLellan, K. M., Maeshima, K., Frangakis, A. S. and Dubochet, J. Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ. Proc. Natl. Acad. Sci. USA 105, 19732-19737 (2008).
16. Naumova, N. et al. Organization of the mitotic chromosome. Science 342, 948-953 (2013
17. Caravaca, J. M., Cano, S., Gallego, I. and Daban, J. R. Structural elements of bulk chromatin within metaphase chromosomes. Chromosome Res. 13, 725-743 (2005).
18. Gallego, I., Castro-Hartmann, P., Caravaca, J. M., Cano, S. and Daban, J. R. Dense chromatin plates in metaphase chromosomes. Eur. Biophys. J. 38, 503-522 (2009).
19. Castro-Hartmann, P., Milla, M. and Daban, J. R. Irregular orientation of nucleosomes in the well-defined chromatin plates of metaphase chromosomes. Biochemistry 49, 4043-4050 (2010).
20. Gallego, I., Oncins, G., Sisquella, X., Fernndez-Busquets, X. and Daban, J. R. Nanotribology results show that DNA forms a mechanically resistant 2D network in metaphase chromatin plates. Biophys. J. 99, 3951-3958 (2010).
21. Milla, M. and Daban, J. R. Self-assembly of thin plates from micrococcal nuclease-digested chromatin of metaphase chromosomes. Biophys. J. 103, 567-575 (2012).
22. Cui, Y. and Bustamante, C. Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. Proc. Natl. Acad. Sci. USA 97, 127-132 (2000).
23. Mihardja, S., Spakowitz, A. J., Zhang, Y. and Bustamante, C. Effect of force on mononucleosomal dynamics. Proc. Natl. Acad. Sci. USA 103, 15871-15876 (2006).
24. Kruithof, M. et al. Single-molecule force spectroscopy reveals a highly compliant helical folding for the 30-nm chromatin fiber. Nat. Struct. Mol. Biol. 16, 534-540 (2009).
25. Poirier, M., Eroglu, S., Chatenay, D. and Marko, J. F. Reversible and irreversible unfolding of mitotic newt chromosomes by applied force. Mol. Biol. Cell 11, 269-276 (2000).
26. Kepper, N. et al. Force spectroscopy of chromatin fibers: extracting energetic and structural information from Monte Carlo simulations. Biopolymers 95, 435-447 (2011).
27. Collepardo-Guevara, R. and Schlick, T. Crucial role of dynamic linker histone binding and divalent ions for DNA accessibility and gene regulation revealed by mesoscale modeling of oligonucleosomes. Nucleic Acids Res. 18, 8803-8817 (2012).
28. Trask, B. J. Human cytogenetics: 46 chromosomes, 46 years and counting. Nature Rev. Genet. 3, 769-778 (2002).
29. Sumner, A. T. Chromosomes. Organization and function (Blackwell, 2003).
30. Shaffer, L. G., McGowan-Jordan, J. and Schmid, M. An international system for human cytogenetic nomenclature (Karger, 2013).
31. Yuris, J. J. Mid-prophase human chromosomes. The attainment of 2000 bands. Hum. Genet. 56, 293-298 (1981).
32. Hliscs, R., Mhlig, P. and Claussen, U. The nature of G-bands analyzed by chromosome stretching. Cytogenet. Cell Genet. 79, 162-166 (1997).
33. The BAC Resource Consortium. Integration of cytogenetic landmarks into the draft sequence of the human genome. Nature 409, 953-958 (2001).
34. Kaiser-Rogers, K. and Rao, K. W. Structural chromosome rearrangements in The principles of clinical cytogenetics (eds Gersen, S. L. and Keagle, M. B.) 139-174 (Springer, 2013).
35. Schrock, E. et al. Multicolor spectral karyotyping of human chromosomes. Science 273, 494-497 (1996).
36. Speicher, M. R., Ballard, S. G. and Ward, D. C. Karyotyping human chromosomes by combinatorial multi-fluor FISH. Nature Genet. 12, 368-375 (1996).
37. Veldman, T., Vignon, C., Schrock, E., Rowley, J. D. and Ried, T. Hidden chromosome abnormalities in haematological malignancies detected by multicolour spectral karyotyping. Nature Genet. 15, 406-410 (1997).
38. Roschke, A. V. et al. Karyotypic complexity of the NCI-60 drug-screening panel. Cancer Res. 63, 8634-8647 (2003).
39. Levy, S. et al. The diploid genome sequence of an individual human. PLoS Biol. 5(10), e254 (2007).
40. Cortes, F. and Escalza, P. Analysis of different banding patterns and late replicating regions in chromosomes of Allium cepa, A. sativum and A. nigrum. Genetica 71, 39-46 (1986).
41. Friebe, B. and Cortes, F. Sister chromatid exchange and replication banding in Plant chromosomes: Laboratory methods (eds Fukui, K. and Nakayama, S.) 171-186 (CRC Press, 1996).
42. Landry, J. J. M. et al. The genomic and transcriptomic landscape of a HeLa cell line. G3: Genes Genomes Genet. 3, 1213-1224 (2013).
43. Lawrence, J. B., Singer, R. H. and McNeil, J. A. Interphase and metaphase resolution of different distances within the human dystrophin gene. Science 249, 928-932 (1990).
44. Saitoh, Y. and Laemmli, U. K. Metaphase chromosome structure: bands arise from a differential folding path of the highly AT-rich scaffold. Cell 76, 609-622 (1994).
45. Nelson, W. G., Pienta, K. J., Barrack, E. R. and Coffey, D. S. The role of the nuclear matrix in the organization and function of DNA. Annu. Rev. Biophys. Biophys. Chem. 15, 457-475 (1986).
46. Trask, B. J. et al. Studies of metaphase and interphase chromosomes using fluorescence in situ hybridization. Cold Spring Harbor Symp. Quant. Biol. 58, 767-775 (1993).
47. Ohnuki, Y. Demonstration of the spiral structure of human chromosomes. Nature 208, 916-917 (1965).
48. Boy de la Tour, E. and Laemmli, U. K. The metaphase scaffold is helically folded: sister chromatids have predominantly opposite helical handedness. Cell 55, 937-944 (1988).
49. Baumgartner, M. et al. Genes occupy a fixed and symmetrical position in sister chromatids. Cell 64, 761-766 (1991).
50. Chen, S. H., Chan, N. L. and Hsieh, T. New mechanistic and functional insights into DNA topoisomerases. Annu. Rev. Biochem. 82, 139-170 (2013).
51. Salceda, J., Fernandez, X. and Roca, J. Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA. EMBO J. 25, 2575-2583 (2006).
52. Chen, T., Sun, Y., Ji, P., Kopetz, S. and Zhang, W. Topoisomerase IIα in chromosome instability and personalized cancer therapy. Oncogene doi: 10.1038/onc.2014.332 (2014).
53. Poirier, M. G., Monhait, T. and Marko, J. F. Reversible hypercondensation and decondensation of mitotic chromosomes studied using combined chemical-micromechanical techniques. J. Cell Biochem. 85, 422-434 (2002).
54. Christensen, M. O. et al. Dynamics of human DNA topoisomerases IIα and IIβ in living cells. J. Cell Biol. 157, 31-44 (2002).
55. Tavormina, P. A. et al. Rapid exchange of mammalian topoisomerase IIα at kinetochores and chromosome arms in mitosis. J. Cell Biol. 158, 23-29 (2002).
56. Comings, D. E. Mechanisms of chromosome banding and implications for chromosome structure. Annu. Rev. Genet. 12, 25-46 (1978).
57. Mitelman, F., Johansson, B. and Mertens, F. Mitelman database of chromosome aberrations and gene fusions in cancer (2015). Available at: http://cgap.nci.nih.gov/Chromosomes/Mitelman. Date of access: 06/08/15.
58. Cell Line NCI60 Drug Discovery Panel. Available at: http://home.ncifcrf.gov/CCR/60SKY/new/demo1.asp. Date of access: 06/08/15.
59. Edwards, P. SKY karyotypes and FISH analysis of epithelial cancer cell lines. Available at: http://www.path.cam.ac.uk/~pawefish. Date of access: 06/08/15.
60. Popp, S. et al. Genetic characterization of a human skin carcinoma progression model: from primary tumor to metastasis. J. Invest. Dermatol. 115, 1095-1103 (2000).
61. Gisselsson, D. et al. Chromosomal breakage-fusion-bridge events cause genetic intratumor heterogeneity. Proc. Natl. Acad. Sci. USA 97, 5357-5362 (2000).
62. Daban, J. R. Physical constraints in the condensation of eukaryotic chromosomes. Local concentration of DNA versus linear packing ratio in higher order chromatin structures. Biochemistry 39, 3861-3866 (2000).