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

Journal of Cell Biology

Volumn 140, Issue 6, 1998, Pages 1285-1295

  Jackson, Dean A ^a   Pombo, Ana ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL CYCLE S PHASE; CELL NUCLEUS; CELL PROLIFERATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA SYNTHESIS; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REPLICON;

ANTIMETABOLITES; BROMODEOXYURIDINE; CELL DIVISION; CELL NUCLEUS; CHROMOSOMES; DNA; DNA REPLICATION; HELA CELLS; HUMANS; IDOXURIDINE; REPLICON; S PHASE;

EID: 0032559794     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.140.6.1285     Document Type: Article

References (59)

1. Abney, J.R., B. Cutler, M.L. Fillbach, D. Axelrod, and B.A. Scalettar. 1997. Chromatin dynamics in interphase nuclei and its implications for nuclear structure. J. Cell Biol. 137:1454-1468.
2. Baumgartner, M., B. Dutrillaux, N. Lemieux, D. Paulin, and E. Viegas-Pequignot. 1991. Genes occupy a fixed and symmetrical position on sister chromatids. Cell. 64:761-767.
3. Berezney, R., M.J. Mortillaro, H. Ma, X. Wei, and J. Samarabandu. 1995a. The nuclear matrix: a structural milieu for genomic function. Int. Rev. Cytol. 162: 1-65.
4. Berezney, R., H. Ma, C. Meng, J. Samarabandu, and P.C. Cheng. 1995b. Connecting genomic architecture and DNA replication in three dimensions. Zool. Studies. 1(Suppl.):29-32.
5. Cocker, J.H., S. Piatti, C. Santocanale, K. Nasmyth, and J.F.X. Diffley. 1996. An essential role for the Cdc6 protein in forming the pre-replicative complexes of budding yeast. Nature. 379:180-182.
6. Cook, P.R. 1995. A chromomeric model for nuclear and chromosome structure. J. Cell Sci. 108:2927-2935.
7. Coverley, D., and R.A. Laskey. 1994. Regulation of eukaryotic DNA replication. Annu. Rev. Biochem. 63:745-776.
8. Cremer, T., A. Kurz, R. Zirbel, S. Dietzel, B. Rinke, E. Schrock, M.R. Speicher, U. Mathieu, A. Jauch, P. Emmerich, et al. 1993. Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harbor Symp. Quant. Biol. 58:777-792.
9. DePamphilis, M.L. 1996. Replication origins in metazoan chromosomes. In Eukaryotic DNA Replication. J.J. Blow, editor. IRL Press, Oxford. 96-123.
10. Diffley, J.F.X., and J.H. Cocker. 1992. Protein-DNA interactions at a yeast replication origin. Nature. 357:169-172.
11. Dolbeare, F. 1995. Bromodeoxyuridine: a diagnostic tool in biology and medicine. Part I. Historical perspectives, histochemical methods and cell kinetics. Histochem. J. 27:334-369.
12. Dolbeare, F. 1996. Bromodeoxyuridine: a diagnostic tool in biology and medicine. Part III. Proliferation in normal, injured and diseased tissue, growth factors, differentiation, DNA replication sites and in situ hybridization. Histochem. J. 28:531-575.
13. Drouin, R., G.P. Holmquist, and C.-L. Richer. 1994. High-resolution replication bands compared with morphologic G- and R-bands. Adv. Hum. Genet. 22:47-115.
14. Earnshaw, W.C. 1988. Mitotic chromosome structure. Bioessays. 9:147-150.
15. Edenberg, H.J., and J.A. Huberman. 1975. Eukaryotic chromosome replication. Annu. Rev. Genet. 9:245-284.
16. Fangman, W.L., and B.J. Brewer. 1992. A question of time: replication origins of eukaryotic chromosomes. Cell. 71:363-366.
17. Fox, M.H., D.J. Arndt-Jovin, T.M. Jovin, P.H. Baumann, and M. Robert-Nicaud. 1991. Spatial and temporal distribution of DNA replication sites localized by immunofluorescence and confocal microscopy. J. Cell Sci. 99:247-255.
18. Fransz, F.F., C. Alonso-Blanco, T.B. Liharska, A.J.M. Peeters, P. Zabel, and J.H. de Jong. 1996. High-resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibers. Plant J. 9:421-130.
19. Hand, R. 1978. Eukaryotic DNA: organization of the genome for replication. Cell. 15:317-325.
20. Hatton, K.S., V. Dhar, E.H. Brown, M.A. Iqbal, S. Stuart, V.T. Didamo, and C.L. Schildkraut. 1988. Replication program of active and inactive multigene families in mammalian cells. Mol. Cell. Biol. 8:2149-2158.
21. Heichman, K.A., and J.M. Roberts. 1994. Rules to replicate by. Cell. 79:557-562.
22. Holmquist, G.P. 1992. Chromosome bands, their chromatin flavors, and their functional features. Am. J. Hum. Genet. 51:17-37.
23. Hozák, P., A.B. Hassan, D.A. Jackson, and P.R. Cook. 1993. Visualization of replication factories attached to a nucleoskeleton. Cell. 73:361-373.
24. Hsiao, C.-L., and J. Carbon. 1979. High-frequency transformation of yeast by plasmids containing the yeast ARG4 gene. Proc. Natl. Acad. Sci. USA. 76: 3829-3833.
25. Huberman, J.A., and A.D. Riggs. 1968. On the mechanism of DNA replication in mammalian chromosomes. J. Mol. Biol. 32:327-341.
26. Humbert, C., and Y. Usson. 1992. Eukaryotic DNA replication is a topologically ordered process. Cytometry. 13:603-614.
27. Jackson, D.A. 1995a. S phase progression in synchronized human cells. Exp. Cell Res. 220:62-70.
28. Jackson, D.A. 1995b. Nuclear organization: uniting replication foci, chromatin domains and chromosome structure, Bioessays. 17:587-591.
29. Jackson, D.A. and P.R. Cook. 1985. A general method for preparing chromatin containing intact DNA. EMBO (Eur. Mol. Biol. Organ.) J. 4:913-918.
30. Kill, I.R., J.M. Bridger, K.H.S. Campbell, G. Maldonado-Codina, and C.J. Hutchison. 1991. The timing of the formation and usage of replicase clusters in S phase nuclei of human diploid fibroblasts. J. Cell Sci. 100:869-876.
31. Kitsberg, D., S. Selig, I. Keshet, and H. Cedar. 1993. Replication structure of the human β-globin gene domain. Nature. 366:506-507.
32. Krude, T. 1995. Chromatin assembly factor 1 (CAF-1) colocalizes with replication foci in HeLa cell nuclei. Exp. Cell Res. 220:304-311.
33. Leonhardt, H., A.W. Page, H.-U. Weier, and T.H. Bestor. 1992. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell. 71:865-873.
34. Lestou, V.S., S. Strehl, T. Lion, H. Gadner, and P.F. Ambros. 1996. High-resolution FISH of the entire integrated Epstein-Barr virus genome on extended human DNA. Cytogenet. Cell Genet. 74:211-217.
35. Manders, E.M.M., J. Slap, G.J. Brakenhoff, R. van Driel, and J.A. Aten. 1992. Dynamics of three-dimensional replication patterns during the S phase, analyzed by double labelling of DNA and confocal microscopy. J. Cell Sci. 103: 857-862.
36. Manders, E.M.M., J. Slap, J. Strackee, R. van Driel, and J.A. Aten. 1996. Dynamic behaviour of DNA replication domains. Exp. Cell Res. 226:328-335.
37. Manuelidis, L. 1985. Individual interphase chromosome domains revealed by in situ hybridization. Hum. Genet. 71:288-293.
38. Manuelidis, L., and T.L. Chen. 1990. A unified model of eukaryolic chromosomes. Cytometry. 11:8-25.
39. Marahrens, Y., and B. Stillman. 1996. The initiation of DNA replication in the yeast Saccharomyces cerevisiae. In Eukaryotic DNA Replication. J.J. Blow, editor, IRL Press, Oxford. 66-95.
40. Morton, N.E. 1991. Parameters of the human genome. Proc. Natl. Acad. Sci. USA. 88:7474-7476.
41. Nakamura, H., T. Morita, and C. Sato. 1986. Structural organisation of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp. Cell Res. 165:291-297.
42. Nurse, P. 1994. Ordering S phase and M phase in the cell cycle. Cell. 79:547-550.
43. O'Keefe, R.T., S.C. Henderson, and D.L. Spector. 1992. Dynamic organization of DNA replication in mammalian cell nuclei: Spatially and temporally defined replication of chromosome-specific α-satellite DNA sequences. J. Cell Biol. 116:1095-1110.
44. Pardoll, D.M., B. Vogelstein, and D.S. Coffey. 1980. A fixed site of DNA replication in eukaryotic cells. Cell. 19:527-536.
45. Parra, I., and B. Windle. 1993. High resolution visual mapping of stretched DNA by fluorescent hybridization. Nat. Genet. 5:17-21.
46. Pombo, A., J. Ferreira, E. Bridge, and M. Carmo-Fonseca. 1994. Adenovirus replication and transcription sites are spatially separated in the nucleus of infected cells. EMBO (Eur. Mol. Biol. Organ.) J. 13:5075-5085.
47. Reynolds, A.E., R.M. McCarroll, C.S. Newlon, and W.L. Fangman. 1989. Time of replication of ARS elements along yeast chromosome III. Mol. Cell. Biol. 9:4488-1494.
48. Saitoh, N., and U.K. Laemmli. 1994. Metaphase chromosome structure: bands arise from a differential folding path of the highly AT-rich scaffold. Cell. 76: 609-622.
49. Schardin, M., T. Cremer, H.D. Hager, and M. Lang. 1985. Specific staining of human chromosomes in Chinese hamster x man hybrid cell lines demonstrates interphase chromosome territories. Hum. Genet. 71:281-287.
50. Selig, S., K. Okumura, D.C. Ward, and H. Cedar. 1992. Delineation of DNA replication time zones by fluorescence in situ hybridization. EMBO (Eur. Mol. Biol. Organ.) J. 11:1217-1225.
51. Sparvoli, E., M. Levi, and E. Rossi. 1994. Replicon clusters may form structurally stable complexes of chromatin and chromosomes. J. Cell Sci. 107:3097-3103.
52. Stinchcomb, D.T., K. Struhl, and R.W. Davis. 1979. Isolation and characterisation of a yeast chromosomal replicator. Nature. 282:39-43.
53. Sumner, A.I. 1991. Scanning electron microscopy of mammalian chromosomes from prophase to telophase. Chromosoma (Berlin). 100:410-418.
54. Tomilin, N., Y. Rosanov, V. Zenin, V. Bozhkov, and B. Vig. 1993. A new and rapid method for visualising DNA replication in spread DNA by immunofluorescence detection of incorporated 5-iododeoxyuridine. Biochem. Biophys. Res. Commun. 190:257-262.
55. Tomilin, N., L. Solovjeva, R. Krutilina, C. Chamberland, R. Hancock, and B. Vig. 1995. Visualization of elementary DNA replication units in human nuclei corresponding in size to DNA loop domains. Chromosome Res. 3:32-10.
56. van den Engh, G., R. Sachs, and B.J. Trask. 1992. Estimating genomic distance from DNA sequence location in cell nuclei by a random walk model. Science. 257:1410-1412.
57. van Dierendonck, J.H., R. Keyzer, C.J.H. van de Velde, and C.J. Cornelisse. 1989. Subdivision of S-phase by analysis of nuclear 5-bromo-deoxyuridine staining patterns. Cytometry. 10:143-150.
58. Vogel, W., M. Autenrieth, and K. Mehnert. 1989. Analysis of chromosome replication by a BrdU antibody technique. Chromosoma (Berlin). 98:335-341.
59. Yokota, H., G. van den Engh, J.H. Hearst, R.K. Sachs, and B.J. Trask. 1995. Evidence for the organisation of chromatin in megabase pair-sized loops arranged along a random walk path in the human G0/G1 interphase nucleus. J. Cell Biol. 130:1239-1249.