3D replicon distributions arise from stochastic initiation and domino-like DNA replication progression

Nature Communications

Volumn 7, Issue , 2016, Pages

  Lob D ^a   Lengert, N ^a   Chagin, V O ^a,b   Reinhart, M ^a   Casas Delucchi, C S ^a   Cardoso, M C ^a   Drossel, B ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b INSTITUTE OF CYTOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS AND CELL COMPONENTS; CHROMOSOME; DNA; INHIBITION; PHYSIOLOGICAL RESPONSE;

CELL CYCLE S PHASE; DNA REPLICATION; EUCHROMATIN; HETEROCHROMATIN; HUMAN; HUMAN CELL; MODEL; REPLICON; STOCHASTIC MODEL; ALGORITHM; BIOLOGICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; GENETICS; HELA CELL LINE; MARKOV CHAIN; METABOLISM;

EUKARYOTA;

DNA; EUCHROMATIN; HETEROCHROMATIN;

ALGORITHMS; COMPUTER SIMULATION; DNA; DNA REPLICATION; EUCHROMATIN; HELA CELLS; HETEROCHROMATIN; HUMANS; MODELS, GENETIC; MOLECULAR CONFORMATION; REPLICON; S PHASE; STOCHASTIC PROCESSES;

EID: 84963660265     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11207     Document Type: Article

References (69)

1. Gilbert, D. M. Replication origin plasticity, Taylor-made: inhibition versus recruitment of origins under conditions of replication stress. Chromosoma 116, 341-347 (2007).
2. Blow, J. J., Dutta, A. Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 6, 476-486 (2005).
3. Chagin, V. O., Stear, J. H., Cardoso, M. C. Organization of DNA replication. Cold Spring Harb Perspect Biol 2, a000737 (2010).
4. Jacob, F., Brenner, S., Cuzin, F. On the regulation of DNA replication in bacteria. Cold Spring Harbor Symposia on Quantitative Biology 28, 329-348 (1963).
5. Lygeros, J. et al. Stochastic hybrid modeling of DNA replication across a complete genome. Proc. Natl Acad. Sci. USA 105, 12295-12300 (2008).
6. Spiesser, T. W., Klipp, E., Barberis, M. A model for the spatiotemporal organization of DNA replication in Saccharomyces cerevisiae. Mol. Genet. Genomics 282, 25-35 (2009).
7. Hyrien, O., Marheineke, K., Goldar, A. Paradoxes of eukaryotic DNA replication: MCM proteins and the random completion problem. Bioessays 25, 116-125 (2003).
8. Machida, Y. J., Hamlin, J. L., Dutta, A. Right place, right time, and only once: replication initiation in metazoans. Cell 123, 13-24 (2005).
9. Mechali, M. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 11, 728-738 (2010).
10. Woodfine, K. et al. Replication timing of the human genome. Hum. Mol. Genet. 13, 191-202 (2004).
11. Casas-Delucchi, C. S. et al. Histone acetylation controls the inactive X chromosome replication dynamics. Nat. Commun. 2, 222 (2011).
12. Casas-Delucchi, C. S. et al. Histone hypoacetylation is required to maintain late replication timing of constitutive heterochromatin. Nucleic Acids Res. 40, 159-169 (2012).
13. Hiratani, I. et al. Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 6, e245 (2008).
14. Jun, S., Herrick, J., Bensimon, A., Bechhoefer, J. Persistence length of chromatin determines origin spacing in Xenopus early-embryo DNA replication: quantitative comparisons between theory and experiment. Cell Cycle 3, 211-217 (2004).
15. Berezney, R., Dubey, D. D., Huberman, J. A. Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma 108, 471-484 (2000).
16. Aladjem, M. I., Fanning, E. The replicon revisited: an old model learns new tricks in metazoan chromosomes. EMBO Rep. 5, 686-691 (2004).
17. Sporbert, A., Gahl, A., Ankerhold, R., Leonhardt, H., Cardoso, M. C. DNA polymerase clamp shows little turnover at established replication sites but sequential de novo assembly at adjacent origin clusters. Mol. Cell 10, 1355-1365 (2002).
18. Guilbaud, G. et al. Evidence for sequential and increasing activation of replication origins along replication timing gradients in the human genome. PLoS Comput. Biol. 7, e1002322 (2011).
19. Cayrou, C. et al. Genome-scale analysis of metazoan replication origins reveals their organization in specific but flexible sites defined by conserved features. Genome Res. 21, 1438-1449 (2011).
20. DePamphilis, M. L. Replication origins in metazoan chromosomes: fact or fiction? Bioessays 21, 5-16 (1999).
21. O'Keefe, R. T., Henderson, S. C., Spector, D. L. Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences. J. Cell Biol. 116, 1095-1110 (1992).
22. Shaw, A., Olivares-Chauvet, P., Maya-Mendoza, A., Jackson, D. A. S-phase progression in mammalian cells: modelling the influence of nuclear organization. Chromosome Res. 18, 163-178 (2010).
23. Takebayashi, S.-I. et al. Regulation of replication at the R/G chromosomal band boundary and pericentromeric heterochromatin of mammalian cells. Exp. Cell Res. 304, 162-174 (2005).
24. Rhind, N. DNA replication timing: random thoughts about origin firing. Nat. Cell Biol. 8, 1313-1316 (2006).
25. Lebofsky, R., Heilig, R., Sonnleitner, M., Weissenbach, J., Bensimon, A. DNA replication origin interference increases the spacing between initiation events in human cells. Mol. Biol. Cell 17, 5337-5345 (2006).
26. Chagin, V. O. et al. 4D Visualization of replication foci in mammalian cells corresponding to individual replicons. Nat. Commun. 7, 11231 (2016).
27. Blow, J. J., Gillespie, P. J., Francis, D., Jackson, D. A. Replication origins in xenopus egg extract are 5-15 kilobases apart and are activated in clusters that fire at different times. J. Cell Biol. 152, 15-26 (2001).
28. Buongiorno-Nardelli, M., Micheli, G., Carri, M. T., Marilley, M. A relationship between replicon size and supercoiled loop domains in the eukaryotic genome. Nature 298, 100-102 (1982).
29. Walter, J., Newport, J. W. Regulation of replicon size in Xenopus egg extracts. Science 275, 993-995 (1997).
30. Courbet, S. et al. Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455, 557-560 (2008).
31. Guillou, E. et al. Cohesin organizes chromatin loops at DNA replication factories. Genes Dev. 24, 2812-2822 (2010).
32. Münkel, C., Langowski, J. Chromosome structure predicted by a polymer model. Phys. Rev. E 57, 5888 (1998).
33. Goldar, A., Labit, H., Marheineke, K., Hyrien, O. A dynamic stochastic model for DNA replication initiation in early embryos. PLoS One 3, e2919 (2008).
34. Gindin, Y., Valenzuela, M. S., Aladjem, M. I., Meltzer, P. S., Bilke, S. A chromatin structure-based model accurately predicts DNA replication timing in human cells. Mol. Syst. Biol. 10, 722 (2014).
35. Yang, S. C.-H. et al. How Xenopus laevis embryos replicate reliably: investigating the random-completion problem. Phys. Rev. E 78, 041917 (2008).
36. Grünwald, D. et al. Probing intranuclear environments at the single-molecule level. Biophys. J. 94, 2847-2858 (2008).
37. Dross, N. et al. Mapping eGFP oligomer mobility in living cell nuclei. PLoS One 4, e5041 (2009).
38. Huberman, J. A., Riggs, A. D. Autoradiography of chromosomal DNA fibers from Chinese hamster cells. Proc. Natl Acad. Sci. USA 55, 599-606 (1966).
39. Dewar, J. M., Walter, J. C. Chromosome biology: conflict management for replication and transcription. Curr. Biol. 23, R200-R202 (2013).
40. Pomerantz, R. T., O'Donnell, M. What happens when replication and transcription complexes collide? Cell Cycle 9, 2537-2543 (2010).
41. Cremer, T., Cremer, C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2, 292-301 (2001).
42. Pope, B. D. et al. Topologically associating domains are stable units of replication-timing regulation. Nature 515, 402-405 (2014).
43. Jackson, D. A., Pombo, A. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 140, 1285-1295 (1998).
44. Consortium, E. P. et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
45. Watanabe, Y. et al. Chromosome-wide assessment of replication timing for human chromosomes 11q and 21q: disease-related genes in timing-switch regions. Hum. Mol. Genet. 11, 13-21 (2002).
46. Manders, E. M., Stap, J., Brakenhoff, G. J., van Driel, R., Aten, J. A. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J. Cell Sci. 103(Pt 3): 857-862 (1992).
47. Nakamura, H., Morita, T., Sato, C. Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp. Cell Res. 165, 291-297 (1986).
48. Nakayasu, H., Berezney, R. Mapping replicational sites in the eucaryotic cell nucleus. J. Cell Biol. 108, 1-11 (1989).
49. Cardoso, M. C., Leonhardt, H., Nadal-Ginard, B. Reversal of terminal differentiation and control of DNA replication: cyclin A and Cdk2 specifically localize at subnuclear sites of DNA replication. Cell 74, 979-992 (1993).
50. Leonhardt, H. et al. Dynamics of DNA replication factories in living cells. J. Cell Biol. 149, 271-280 (2000).
51. Bohn, M., Heermann, D. W., van Driel, R. Random loop model for long polymers. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 76, 051805 (2007).
52. Mateos-Langerak, J. et al. Spatially confined folding of chromatin in the interphase nucleus. Proc. Natl Acad. Sci. USA 106, 3812-3817 (2009).
53. Parada, L., Misteli, T. Chromosome positioning in the interphase nucleus. Trends Cell Biol. 12, 425-432 (2002).
54. Bolzer, A. et al. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol. 3, e157 (2005).
55. Dreszer, T. R. et al. The UCSC Genome Browser database: extensions and updates 2011. Nucleic Acids Res. 40, D918-D923 (2012).
56. Lucas, I., Chevrier-Miller, M., Sogo, J. M., Hyrien, O. Mechanisms ensuring rapid and complete DNA replication despite random initiation in Xenopus early embryos. J. Mol. Biol. 296, 769-786 (2000).
57. Duan, Z., Blau, C. A. The genome in space and time: does form always follow function? Bioessays 34, 800-810 (2012).
58. Sachs, R., Van Den Engh, G., Trask, B., Yokota, H., Hearst, J. A random-walk/giant-loop model for interphase chromosomes. Proc. Natl Acad. Sci. USA 92, 2710-2714 (1995).
59. Goldar, A., Marsolier-Kergoat, M.-C., Hyrien, O. Universal temporal profile of replication origin activation in eukaryotes. PLoS One 4, e5899 (2009).
60. Jun, S., Zhang, H., Bechhoefer, J. Nucleation and growth in one dimension. I. The generalized Kolmogorov-Johnson-Mehl-Avrami model. Phys. Rev. E 71, 011908 (2005).
61. Bechhoefer, J., Marshall, B. How Xenopus laevis replicates DNA reliably even though its origins of replication are located and initiated stochastically. Phys. Rev. Lett. 98, 098105 (2007).
62. Bickmore, W. A., Carothers, A. D. Factors affecting the timing and imprinting of replication on a mammalian chromosome. J. Cell Sci. 108(Pt 8): 2801-2809 (1995).
63. Earnshaw, W. C., Laemmli, U. K. Architecture of metaphase chromosomes and chromosome scaffolds. J. Cell Biol. 96, 84-93 (1983).
64. Paulson, J. R., Laemmli, U. The structure of histone-depleted metaphase chromosomes. Cell 12, 817-828 (1977).
65. Jackson, D., Dickinson, P., Cook, P. The size of chromatin loops in HeLa cells. EMBO J. 9, 567 (1990).
66. Ganai, N., Sengupta, S., Menon, G. I. Chromosome positioning from activity-based segregation. Nucleic Acids Res. 42, 4145-4159 (2014).
67. Drouin, R., Lemieux, N., Richer, C. L. Analysis of DNA replication during S-phase by means of dynamic chromosome banding at high resolution. Chromosoma 99, 273-280 (1990).
68. Rego, A., Sinclair, P. B., Tao, W., Kireev, I., Belmont, A. S. The facultative heterochromatin of the inactive X chromosome has a distinctive condensed ultrastructure. J. Cell Sci. 121, 1119-1127 (2008).
69. Reinhart,M., Casas-Delucchi, C. S., Cardoso, M. C. Spatiotemporal visualization of DNA replication dynamics. Imaging Gene Expr. 1042, 213-225 (2013).