Association of chromosome territories with the nuclear matrix: Disruption of human chromosome territories correlates with the release of a subset of nuclear matrix proteins

Journal of Cell Biology

Volumn 146, Issue 3, 1999, Pages 531-541

  Ma, Hong ^a,b   Siegel, Alan J ^a   Berezney, Ronald ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Chromosome painting; Chromosome territory; DNA rich nuclear matrix; Fluorescence in situ hybridization; Nuclear matrix proteins

Indexed keywords

ACID PROTEIN; DNA; MATRIX PROTEIN; NUCLEAR PROTEIN; NUCLEASE; SODIUM CHLORIDE;

ARTICLE; CELL NUCLEUS MATRIX; CHROMOSOME; CHROMOSOME PAINTING; CONTROLLED STUDY; DNA REPLICATION; FIBROBLAST; FRACTIONATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN SECRETION;

AMMONIUM SULFATE; CELL LINE; CELL NUCLEUS; CHROMOSOME PAINTING; CHROMOSOMES, HUMAN; DISULFIDES; DNA; DNA REPLICATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FIBROBLASTS; HUMANS; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MOLECULAR WEIGHT; NUCLEAR MATRIX; NUCLEAR PROTEINS; OSMOLAR CONCENTRATION; RIBONUCLEASE, PANCREATIC; SODIUM CHLORIDE;

EID: 0033538846     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.146.3.531     Document Type: Article

References (101)

1. Abney, J.R., B. Cutler, M.L. Filibach, D. Axelrod, and B.A. Scalettar. 1997. Chromatin dynamics in interphase nuclei and its implications for nuclear structure. J. Cell Biol. 137:1459-1468.
2. Adachi, Y., E. Kas, and U.K. Laemmli. 1989. Preferential cooperative binding of DNA topoisomerase II to scaffold-associated regions. EMBO (Eur. Mol. Biol. Organ.) J. 13:3997-4006.
3. Adachi, Y., M. Luke, and U.K. Laemmli. 1991. Chromosome assembly in vitro: topoisomerase II is required for condensation. Cell. 64:137-148.
4. Baskin, Y. 1995. Mapping the cell's nucleus. Science. 268:1564-1565.
5. Bass, H.W., W.F. Marshall, J.W. Sedat, D.A. Agard, and W.Z. Cande. 1997. Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J. Cell Biol. 137:5-18.
6. Belgrader, P., A.J. Siegel, and R. Berezney. 1991. A comprehensive study on the isolation and characterization of the HeLa S3 nuclear matrix. J. Cell Sci. 98:281-291.
7. Berezney, R. 1979. Dynamic properties of the nuclear matrix. In The Cell Nucleus. H. Busch, editor. Academic Press, Inc., NY, 413-456.
8. Berezney, R. 1984. Organization and functions of the nuclear matrix. In Chromosomal Nonhistone Proteins. L.S. Hnilica, editor. CRC Press Inc., Boca Raton, FL. 119-180.
9. Berezney, R. 1991. Visualizing DNA replication sites in the cell nucleus. Sem. Cell Biol. 2:103-115.
10. Berezney, R. 1992. The nuclear matrix: structure, function and DNA replication. Adv. Mol. Cell Biol. 4:37-73.
11. Berezney, R., and D.S. Coffey, 1977. Nuclear matrix. Isolation and characterization of a framework structure from rat liver nuclei. J. Cell Biol. 73:616-637.
12. Berezney, R., and L.A. Buchholtz. 1981. Isolation and characterization of rat liver nuclear matrices containing high molecular weight deoxyribonucleic acid. Biochem. 20:4995-5002.
13. Berezney, R., and X. Wei. 1998. The new paradigm: integrating genomic function and nuclear architecture. J. Cell. Biochem. Suppl. 30/31:238-242.
14. Berezney, R., M.J. Mortillaro, H. Ma, X. Wei, and J. Samarabandu. 1995. The nuclear matrix: a structural milieu for genomic function. Int. Rev. Cytol. 162A:1-65.
15. Chai, L.S., and A.A. Sandberg. 1988. Chromosomes and their relationship to nuclear components during the cell cycle in Chinese hamster cells. Cell Tissue Res. 251:197-204.
16. Clemson, C.M., J.A. McNeil, H.F. Willard, and J.B. Lawrence. 1996. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell Biol. 132:259-275.
17. Cook, P.R. 1991. The nucleoskeleton and the topology of replication. Cell. 66: 627-635.
18. Cook, P.R., and I.A. Brazell. 1975. Supercoils in human DNA. J. Cell Sci. 19: 261-279.
19. Cook, P.R., I.A. Brazell, and E. Jost. 1976. Characterization of nuclear structures containing superhelical DNA. J. Cell Sci. 22:303-324.
20. Cremer, T., C. Cremer, and H. Baumann. 1982. Rabl's model of the interphase chromosome arrangement tested in Chinese hamster's cells by premature chromosome condensation and laser-UV-microbeam experiments. Hum. Genet. 60:46-56.
21. Cremer, T., A. Kurz, R. Zirbel, S. Dietzel, B. Rink, 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.
22. Cremer, T., S. Dietzel, R. Eils, P. Lichter, and C. Cremer. 1995. Chromosome territories, nuclear matrix filaments and inter-chromatin channels: a topological view on nuclear architecture and function. In Kew Chromosome Conference. IV. P.E. Brandham and M.D. Bennett, editors. The Royal Botanical Gardens, Kew, Richmond, Surrey, UK. 63-81.
23. de Belle, I., S.T. Cai, and T. Kohwi-Shigematsu, 1998. The genomic sequences bound to special at-rich sequence-binding protein 1 (Satb1) in vivo in Jurkat T cells are tightly associated with the nuclear matrix at the bases of the chromatin loops. J. Cell Biol. 141:335-348.
24. De Boni, U., 1994. The interphase nucleus as a dynamic structure. Int. Rev. Cytol. 150:149-171.
25. De Boni, U., and A. Mintz. 1986. Curvilinear, three-dimensional motion of chromatin domains and nucleoli in neuronal interphase nuclei. Science. 234: 863-866.
26. Dickinson, L.A., and T. Kohwi-Shigematsu. 1995. Nucleolin is a matrix attachment region DNA-binding protein that specifically recognizes a region with high base-unpairing potential. Mol. Cell. Biol. 15:456-465.
27. Dickinson, L.A., T. Joh, Y. Kohwi, and T. Kohwi-Shigematsu. 1992. A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell. 70:631-645.
28. Dickinson, L.A., C.D. Dickinson, and T. Kohwi-Shigematsu. 1997. An atypical homeodomain in SATB1 promotes specific recognition of the key structural element in a matrix attachment region. J. Biol. Chem. 272:11463-11470.
29. Dietzel, S., E. Weiland, R. Eils, C. Munkel, C. Cremer, and T. Cremer. 1995. Three-dimensional distribution of centromeric or paracentromeric heterochromatin of chromosomes 1,7.15 and 17 in human lymphocyte nuclei studied with light microscopic axial tomography. Bioimaging. 3:121-133.
30. Dietzel, S., A. Jauch, D. Kienle, G. Ou, H. Holtgreve-Grez, R. Eils, F.C. Munkel, M. Bittner, P.S. Meltzer, J.M. Trent, et al. 1998. Separate and variably shaped chromosome arm domains are disclosed by chromosome arm painting in human cell nuclei. Chromosome Res. 6:25-33.
31. Dijkwel, P.A., L.H. Mullenders, and F. Wanka. 1979. Analysis of the attachment of replicating DNA to a nuclear matrix in mammalian interphase nuclei. Nucleic Acids Res. 6:219-230.
32. Elis, R.S., S. Dietzel, E. Bertin, E. Schrock, M.R. Speicher, T. Reid, M. Robert-Nicoud, C. Cremer, and T. Cremer. 1996. Three-dimensional reconstruction of painted human interphase chromosomes: active and inactive × chromosome territories have similar volumes but differ in shape and surface structure. J Cell Biol. 135:1427-1440.
33. Fackelmayer, F.O., K. Dahm, A. Renz, U. Ramsperger. and A. Richter. 1994. Nucleic-acid-binding properties of hnRNP-U/SAF-A, a nuclear matrix protein which binds DNA and RNA in vivo and in vitro. Eur. J. Biochem. 221: 749-757.
34. Ferguson, M., and D.C. Ward. 1992. Cell cycle dependent chromosomal movement in pre-mitotic human T-lymphocyte nuclei. Chromosoma. 101:557-565.
35. Fey, E.G., G. Krochmalnic, and S. Penman. 1986. The nonchromatin substructures of the nucleus: the ribonucleoprotein (RNP)-containing and RNP-depleted matrices analyzed by sequential fraction and resinless section electron microscopy. J Cell Biol. 102:1654-1665.
36. Funabiki, H., I. Hagan, S. Uzawa, and M. Yanagida. 1993. Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J. Cell Biol. 121:961-976.
37. Gasser, S.M., and U.K. Laemmli. 1987. A glimpse of chromosomal order. Trends Gen. 3:16-21.
38. Gerdes, M.G., K.C. Carter, P.T. Moen, Jr., and J.B. Lawrence. 1994. Dynamic changes in the higher-level chromatin organization of specific sequences revealed by in situ hybridization to nuclear halos. J. Cell Biol. 126:289-304.
39. Goldberg, G.I., I. Collier, and A. Cassel. 1983. Specific DNA sequences associated with the nuclear matrix in synchronized mouse 3T3 cells. Proc. Natl. Acad. Sci. USA. 80:6887-6891.
40. Hand, R. 1978. Eucaryotic DNA: organization of the genome for replication. Cell. 15:315-325.
41. He, D., J.A. Nickerson, and S. Penman. 1990. Core filaments of the nuclear matrix. J. Cell Biol. 110:569-580.
42. He, D., T. Martin, and S. Penman. 1991. Localization of heterogeneous nuclear ribonucleoprotein in the interphase nuclear matrix core filaments and on perichromosomal filaments at mitosis. Proc. Natl. Acad. Sci. USA. 88:7469-7473.
43. Hernandez-Verdun, D., and T. Gautier. 1994. The chromosome periphery during mitosis. Bioessays. 16:179-185.
44. Hirano, T., and T.J. Mitchison. 1994. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell. 79:449-458.
45. Hiraoka, Y., A.F. Dernburg, S.J. Parmelee, M.C. Rykowski, D.A. Agard, and J.W. Sedat. 1993. The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J. Cell Biol. 120:591-600.
46. Hoffman, M. 1993. The cell's nucleus shapes up. Science. 259:1257-1259.
47. Jackson, D.A., and P.R. Cook. 1995. The structural basis of nuclear function. Int. Rev. Cytol. 162A:125-149.
48. Jackson, D. A., and A. Pombo. 1998. 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.
49. Janevski, J., P.C. Park, and U. De Boni. 1995. Organization of centromeric domains in hepatocyte nuclei: rearrangement association with de novo activation of the vitellogenin gene family in Xenopus laevis. Exp. Cell Res. 217: 227-239.
50. Kaufmann, S.H., D.S. Coffey, and J.H. Shaper 1981. Considerations in the isolation of rat liver nuclear matrix, nuclear envelope, and pore complex lamina. Exp. Cell Res. 132:105-123.
51. Laemmli, U.K., E. Kas, L. Poljak, and Y. Adachi. 1992. Scaffold-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr. Opin. Gen. Dev. 2:275-285.
52. LaSalle, J.M., and M. Lalande. 1996. Homologous association of oppositely imprinted chromosomal domains. Science. 272:725-728.
53. Lebkowski, J.S., and U.K. Laemmli. 1982. Evidence for two levels of DNA folding in histone-depleted HeLa interphase nuclei. J. Mol. Biol. 156:309-324.
54. Leitch, A.R., W. Mosgoller, T. Schwarzacher, M.D. Bennett, and J.S. Heslop-Harrison 1990. Genomic in situ hybridization to sectioned nuclei shows chromosome domains in grass hybrids. J. Cell Sci. 95:335-341.
55. Lichter, P., T. Cremer, J. Borden, L. Manuelidis, and D.C. Ward. 1988. Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombination DNA libraries. Hum. Genet. 80:224-234.
56. Liu, J., D. Bramblett, Q. Zhu, M. Lozano, R. Kobayashi, S.R. Ross, and J.P. Dudley. 1997. The matrix attachment region-binding protein SATB1 participates in negative regulation of tissue-specific gene expression. Mol. Cell. Biol. 17:5275-5287.
57. Luderus, M.E.E., A. de Graaf, E. Mattia, J.L. den Blaauwen, M.A. Grande, L. de Jong, and R. van Driel. 1992. Binding of matrix attachment regions to lamin B1. Cell. 70:949-959.
58. Luderus, M.E.E., J.L. den Blaauwen, O.J. de Smit, D.A. Compton, and R. van Driel. 1994. Binding of matrix attachment regions to lamin polymers involves single-stranded regions and the minor groove. Mol Cell. Biol. 14: 6297-6305.
59. Ma, H., J. Samarabandu, R.S. Devdhar, R. Acharya, P.-C. Cheng, C. Meng, and R. Berezney. 1998. Spatial and temporal dynamics of DNA replication sites in mammalian cells. J. Cell Biol. 143:1415-1425.
60. Manuelidis, L. 1985. Individual interphase chromosome domains revealed by in situ hybridization. Hum. Genet. 71:288-293.
61. Manuelidis, L. 1990. A view of interphase chromosomes. Science. 250:1533-1540.
62. McCready, S.J., A. Akrigg, and P.R. Cook. 1979. Electron-microscopy of intact nuclear DNA from human cells. J. Cell Sci. 39:53-62.
63. Mortillaro, M., and R. Berezney. 1998. Matrin CyP, an SR-rich cyclophilin that associates with the nuclear matrix and splicing factors. J. Biol. Chem. 273: 8188-8192.
64. Mortillaro, M., B.J. Blencowe, X. Wei, H. Nakayasu, L. Du, S.L. Warren, P.A. Sharp, and R. Berezney. 1996. A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix. Proc. Natl. Acad. Sci. USA. 93:8253-8257.
65. Nakayasu, H., and R. Berezney. 1989. Mapping replicational sites in the eucaryotic cell nucleus. J. Cell Biol. 108:1-11.
66. Nakayasu, H., and R. Berezney. 1991. Nuclear matrins: identification of the major nuclear matrix proteins. Proc. Natl. Acad. Sci. USA. 88:10312-10316.
67. Nagele, R., T. Freeman, L. McMorrow, and H-Y. Lee. 1995. Precise spatial positioning of chromosomes during premetaphase: evidence for chromosomal order. Science. 270:1831-1834.
68. Nelson, W.G., and D.S. Coffey. 1987. Structural aspects of mammalian DNA replication: topoisomerase II. NCI (Natl. Cancer Inst.) Monogr. 4:23-29.
69. Neri, L.M., G. Mazzotti, S. Capitani, N.M. Maraldi, C. Cinti, N. Baldini, R. Rana, and A.M. Martelli. 1992. Nuclear matrix-bound replicational sites detected in situ by 5-bromodeoxyuridine. Histochem. 98:19-32.
70. Nickerson, J.A., B.J. Blencowe, and S. Penman. 1995. The architectural organization of nuclear metabolism. Int. Rev. Cytol. 162A:67-123.
71. Pardoll, D.M., B. Vogelstein, and D.S. Coffey. 1980. A fixed site of DNA replication in eucaryotic cells. Cell. 19:527-536.
72. Park, P.C., and U. De Boni. 1998. A specific conformation of the territory of chromosome 17 locates ERBB-2 sequences to a DNase-hypersensitive domain at the nuclear periphery. Chromosoma. 107:87-95.
73. Paulson, J.R., and U.K. Laemmli. 1977. The structure of histone-depleted metaphase chromosomes. Cell. 12:817-828.
74. Pienta, K.J., and D.S. Coffey. 1984. A structural analysis of the role of the nuclear matrix and DNA loops in the organization of the nucleus and chromosome. J. Cell Sci. Suppl. 1:123-135.
75. Pinkel, D., J. Landegent, and C. Collins. 1988. Fluorescence in situ hybridization with human chromosome-specific libraries: detection of trisomy 21 and translocations of chromosome 4. Proc. Natl. Acatl. Sci. USA. 85:9138-9142.
76. Pluta, A.F., A.M. Mackay, A.M. Anisztein, I.G. Goldberg, and W.C. Earnshaw. 1995. The centromere: hub of chromosomal activities. Science. 270:1519-1594.
77. Reyes, J.C., C. Muchardt, and M. Yaniv. 1997. Components of the human SWI/ SNF complex are enriched in active chromatin and are associated with the nuclear matrix. J. Cell Biol. 137:263-274.
78. Roberge, M., and S.M. Gasser. 1992. DNA loops: structural and functional properties of scaffold-attached regions. Mol. Microbiol. 6:419-423.
79. Romig, H., F.O. Fackelmayer, A. Renz, U. Ramsperger, and A. Richter. 1992. Characterization of SAF-A, a novel nuclear DNA binding protein from HeLa cells with high affinity for nuclear matrix/scaffold attachment DNA elements. EMBO (Eur. Mol. Biol. Organ.) J. 11:3431-3440.
80. Saitoh, N., I.G. Goldberg, E.R. Wood, and W.C. Earnshaw. 1994. ScII: an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure. J. Cell Biol. 127:303-318.
81. Saitoh, Y., 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.
82. 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.
83. Schwarzacher, T. 1994. Mapping in plants: progress and prospects. Curr. Opin. Gen. Dev. 4:868-874.
84. Seksek, O., J. Biwersi, and A.S. Verkman. 1997. Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. J. Cell Biol. 138:131-142.
85. Shelby, R.D., K.M. Hahn, and K.F. Sullivan. 1996. Dynamic elastic behavior of alpha-satellite DNA domains visualized in situ in living human cells. J. Cell Biol. 135:545-557.
86. Shelby, R.D., O. Vafa, and K.F. Sullivan. 1997. Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites. J. Cell Biol. 136:501-513.
87. Smith, H.C., E. Puvion, L.A. Buchholtz, and R. Berezney. 1984. Spatial distribution of DNA loop attachment and replicational sites in the nuclear matrix. J. Cell Biol. 99:1794-1802.
88. Spector, D.L. 1993. Nuclear organization of pre-mRNA processing. Curr. Opin. Cell Biol. 5:442-447.
89. Stack, S.M., D.B. Brown, and W.C. Dewey. 1977. Visualization of interphase chromosomes. J. Cell Biol. 135:545-557.
90. Tsutsui, K., K. Tsutsui, S. Okada, S. Watarai, S. Seki, T. Yasuda, and T. Shohmori. 1993. Identification and characterization of a nuclear scaffold protein that binds the matrix attachment region DNA. J. Biol. Chem. 268:12886-12894.
91. van Driel, R., D.O. Wansink, B. van Steensel, M.A. Grande, W. Schul, and L. de Jong. 1995. Nuclear domains and the nuclear matrix. Int. Rev. Cytol. 162A:151-189.
92. Verheijen, R., H.J. Kuijpers, R. van Driel, J.L. Beck, J.H. van Dierendonck, G.J. Brakenhoff, and F.C. Ramaekers. 1989. Ki-67 detects a nuclear matrix-associated proliferation-related antigen. II. Localization in mitotic cells and association with chromosomes. J. Cell Sci. 92:531-540.
93. Vogelstein, B., D.M. Pardoll, and D.S. Coffey. 1980. Supercoiled loops and eucaryotic DNA replicaton. Cell. 22:79-85.
94. von Kries, J.P., H. Buhrmester, and W.H. Stratling. 1991. A matrix/scaffold attachment region binding protein: identification, purification, and mode of binding. Cell. 64:123-135.
95. Wang, B., L.A. Dickinson, E. Koivunen, E. Ruoslahti, and T. Kohwi-Shigematsu. 1995. A novel matrix attachment region DNA binding motif identified using a random phage peptide library. J. Biol. Chem. 270:23239-23242.
96. Warren, A.C., and P.R. Cook. 1978. Supercoiling of DNA and nuclear conformation during the cell-cycle. J. Cell Sci. 30:211-226.
97. Wei, X., J. Samarabandu, R.S. Devdhar, A.J. Siegel, R. Acharya, and R. Berezney. 1998. Segregation of transcription and replication sites into higher order domains. Science. 281:1502-1504.
98. Wei, X., S. Somananthan, J. Samarabandu, and R. Berezney. 1999. Three dimensional visualization of transcription sites and their association with splicing factor rich nuclear speckles. J. Cell Biol. 146:543-558.
99. Zink, D., and T. Cremer. 1998. Cell nucleus: chromosome dynamics in nuclei of living cells. Curr. Biol. 8:R321-R324.
100. Zink, D., T. Cremer, R. Saffrich, R. Fischer, M.F. Trendelenburg, W. Ansorge, and E.H.K. Stelzer. 1998. Structure and dynamics of human interphase chromosome territories in vivo. Hum. Genet. 102:241-251.
101. Zorn. C., C. Cremer, T. Cremer, and J. Zimmer. 1979. Unscheduled DNA synthesis after partial UV irradiation of the cell nucleus. Exp. Cell Res. 124: 111-119.