The controversial nuclear matrix: A balanced point of view

Histology and Histopathology

Volumn 17, Issue 4, 2002, Pages 1193-1205

  Martelli, Alberto M ^a   Falcieri, E ^a   Zweyer, M ^a   Bortul, R ^a   Tabellini, G ^a   Cappellini, A ^a   Cocco, L ^a   Manzoli, L ^a  

^a Depto Anat Umane Fisiopatologia   (Italy)

Author keywords

Function; Nucleus; Protein; Skeleton; Structure

Indexed keywords

ACTIN; MATRIX PROTEIN; NONHISTONE PROTEIN; RIBONUCLEASE; RIBONUCLEOPROTEIN;

APOPTOSIS; CELL FRACTIONATION; CELL ISOLATION; CELL NUCLEUS INCLUSION BODY; CELL NUCLEUS MATRIX; CELL ORGANELLE; CELL STRUCTURE; CHROMATIN STRUCTURE; CYTOSKELETON; DISULFIDE BOND; ENVELOPE GENE; EXTRACTION; HUMAN; IMMUNOCYTOCHEMISTRY; ISOLATION PROCEDURE; MOLECULAR STABILITY; MORPHOLOGY; NONHUMAN; REVIEW; STRUCTURE ANALYSIS; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; CELL NUCLEUS; HUMANS; NUCLEAR MATRIX; NUCLEAR PROTEINS; TISSUE FIXATION;

EID: 0036791884     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (89)

1. Adolph K. (1980). Organization of chromosomes in HeLa cells: isolation of histone-depleted nuclei and nuclear scaffolds. J. Cell Sci. 42, 291-294.
2. Arends M.J., Morris R.G. and Wyllie A.H. (1990). Apoptosis. The role of endonuclease. Am. J. Pathol. 136, 593-608.
3. Bazett-Jones D.P. and Hendzel M.J. (1999). Electron spectroscopic imaging of chromatin. Methods 17, 188-200.
4. Belgrader P., Siegel A.J. and Berezney R. (1991). A comprehensive study on the isolation and characterization of the HeLa S3 nuclear matrix. J. Cell Sci. 98, 281-291.
5. Berezney R. (1991). The nuclear matrix: a heuristic model for investigating genomic organization and function in the cell nucleus. J. Cell. Biochem. 47, 109-123.
6. Berezney R. and Coffey D.S. (1974). Identification of a nuclear protein matrix. Biochem. Biophys. Res. Commun. 60, 1410-1417.
7. Berezney R. and Coffey D.S. (1975). Nuclear protein matrix: association with newly-synthesized DNA. Science 189, 291-292.
8. Berezney R., Mortillaro M., Ma H., Meng C., Samarabandu J., Wei X., Somanathan S., Liou W.S., Pan S.J. and Cheng P. (1996). Connecting nuclear architecture and genomic function. J. Cell Biochem. 62, 223-226.
9. Berrios S. and Fisher P.A. (1988). Thermal stabilization of putative karyoskeletal protein-enriched fractions from Saccharomyces cerevisiae. Mol. Cell. Biol. 8, 4573-4575.
10. Broers J.L.V., Machiels B.M., van Eys G.J.J.M., Kuijpers H.J.H., Manders E.M.M., van Driel R. and Ramaekers F.C.S. (1999). Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J. Cell Sci. 112, 3463-3475.
11. Capco D.G., Wan K.M. and Penman S. (1982). The nuclear matrix: three-dimensional architecture and protein composition. Cell 29, 847-858.
12. Casiano C.A., Martin S.J., Green D.R. and Tan E.M. (1996). Selective cleavage of nuclear autoantigens during CD95(Fas/APO-1)-mediated T cell apoptosis. J. Exp. Med. 184, 765-770.
13. Counis M.F. and Torriglia A. (2000). DNases and apoptosis. Biochem. Cell Biol. 78, 405-414.
14. Djondjurov L., Ivanova E., Markov D., Bardarov S. and Sachsenmaier W. (1986). Is the nuclear matrix the site of DNA replication in eukaryotic cells? Exp. Cell Res. 164, 79-96.
15. Dundr M. and Misteli T. (2001). Functional architecture in the cell nucleus. Biochem. J. 356, 297-310.
16. Durrieu F., Samejina K., Fortune J.M., Kandels-Lewis S., Osheroff N. and Earnshaw W.C. (2000). DNA topoisomerase IIα interacts with CAD nuclease and is involved in chromatin condensation during apoptotic execution. Curr. Biol. 10, 923-926.
17. Dynlacht J.R., Earles M., Henthorn J., Roberts Z.V., Howard E.W., Seno J.D., Sparling D. and Story M.D. (1999). Degradation of the nuclear matrix is a common element during radiation-induced apoptosis and necrosis. Radiat. Res. 152, 590-603.
18. Earnshaw W.C. (1995). Nuclear changes in apoptosis. Curr. Biol. 7, 337-343.
19. Earnshaw W.C., Martins L.M. and Kaufmann S.H. (1999). Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 68, 383-424.
20. Gerner C., Holzmann K., Meissner M., Gotzmann J., Grimm R. and Sauermann G. (1999). Reassembling proteins and chaperones in human nuclear matrix protein fractions. J. Cell. Biochem. 74, 145-151.
21. Göhring F., Schwab B.L., Nicotera P., Leist M. and Fackelmayer F.O. (1997). The novel SAR-binding domain of scaffold attachment factor A (SAF-A) is a target in apoptotic nuclear breakdown. EMBO J. 16, 7361-7371.
22. Gotzmann J., Vicek S. and Foisner R. (2000). Caspase-mediated cleavage of the chromosome-binding domain of lamina-associated polypeptide 2a. J. Cell Sci. 113, 3769-3780.
23. Gueth-Hallonet C., Weber K. and Osborn M. (1997). Cleavage of the nuclear matrix protein NuMA during apoptosis. Exp. Cell Res. 233, 21-24.
24. Gueth-Hallonet C., Wang J., Harborth J., Weber K. and Osborn M. (1998). Induction of a regular nuclear lattice by overexpression of NuMA. Exp. Cell Res. 243, 434-452.
25. Hancock R. (2000). A new look at the nuclear matrix. Chromosoma 109, 219-225.
26. Harborth J., Wang J., Gueth-Hallonet C., Weber K. and Osborn M. (1999). Self assembly of NuMA: multiarm oligomers as structural units of a nuclear lattice. EMBO J. 18, 1689-1700.
27. He D.C., Nickerson J.A. and Penman S. (1990). Core filaments of the nuclear matrix. J. Cell Biol. 110, 569-580.
28. Hengartner M.O. (2000). The biochemistry of apoptosis. Nature 407, 770-776.
29. Hendzel M.J., Boisvert F.-M. and Bazett-Jones D.P. (1999). Direct visualization of a protein nuclear architecture. Mol. Biol. Cell 10, 2051-2062.
30. Hozak P., Sasseville A.M., Raymond Y. and Cook P.R. (1995). Lamin proteins form an internal nucleoskeleton as well as a peripheral lamina in human cells. J. Cell Sci. 108, 635-644.
31. Izaurralde E., Kas E. and Laemmli U.K. (1989). Highly preferential nucleation of histone H1 assembly on scaffold-associated regions. J. Mol. Biol. 210, 573-585.
32. Izaurralde E., Mirkovitch J. and Laemmli U.K. (1988). Interaction of DNA with nuclear scaffolds in vitro. J. Mol. Biol. 200, 111-125.
33. Jackson D.A. and Cook P.R. (1988). Visualization of a filamentous nucleoskeleton with a 23 nm axial repeat. EMBO J. 7, 3667-3677.
34. Jackson D.A. and Cook P.R. (1995). The structural basis of nuclear function. Int. Rev. Cytol. 162A, 125-149.
35. Jackson D.A., Yuan J. and Cook P.R. (1988). A gentle method for preparing cyto- and nucleo-skeletons and associated chromatin. J. Cell Sci. 90, 365-378.
36. Kaufmann S.H. and Shaper J.H. (1984). A subset of non-histone nuclear proteins stabilized by the sulfhydryl cross-linking reagent tetrathionate. Polypeptides of the internal nuclear matrix. Exp. Cell Res. 155, 477-495.
37. Kaufmann S.H. and Shaper J.H. (1991). Association of topoisomerase II with the hepatoma cell nuclear matrix: the role of intermolecular disulfide bond formation. Exp. Cell Res. 192, 511-523.
38. Kerr J.F.R., Wyllie A.H. and Currie A.R. (1972). Apoptosis: a basic biological phenomenon with wide ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
39. Kipp M., Schwab B.L., Przybylski M., Nicotera P. and Fackelmayer F.O. (2000). Apoptotic cleavage of scaffold attachment factor A (SAF-A) by caspase-3 occurs at a noncanonical cleavage site. J. Biol. Chem. 275, 5031-5036.
40. Kruhlak M.J., Lever M.A., Fischle W., Verdin E., Bazett-Jones D.P. and Hendzel M.J. (2000). Reduced mobility of the ASF splicing factor through the nucleoplasm and steady-state speckle compartments. J. Cell Biol. 150, 41-51.
41. Krystosek A. (1999). Preferential sites of early DNA cleavage in apoptosis and the pathway of nuclear damage. Histochem. Cell Biol. 111, 265-276.
42. Lamond A.I. and Earnshaw W.C. (1998). Structure and function in the nucleus. Science 280, 547-553.
43. Lebkoswki J.S. and Laemmli U.K. (1982). Non-histone proteins and long-range organization of HeLa interphase DNA. J. Mol. Biol. 156, 325-344.
44. Lewis C.D., Lebkowski J.S., Daly A.K. and Laemmli U.K. (1984). Interphase nuclear matrix and metaphase scaffolding structures. J. Cell Sci. Suppl. 1, 103-122.
45. Ma H., Samarabandu J., Devdahr R.S., Acharya R., Cheng P., Meng C. and Berezney R. (1998). Spatial and temporal dynamics of DNA replication sites in mammalian cells. J. Cell Biol. 143, 1415-1425.
46. Ma H., Siegel A.J. and Berezeny R. (1999). Association of chromosome territories with the nuclear matrix: disruption of human chromosome territories correlates with the release of a subset of nuclear matrix proteins. J. Cell Biol. 146, 531-541.
47. Martelli A.M., Gilmour R.S., Falcieri E., Manzoli F.A. and Cocco L. (1990). Temperature-dependent association of DNA polymerase α activity with the nuclear matrix. Exp. Cell Res. 190, 227-232.
48. Martelli A.M., Falcieri E., Gobbi P., Manzoli L., Gilmour R.S. and Cocco L. (1991). Heat-induced stabilization of the nuclear matrix. A biochemical and morphological analysis in mouse erythroleukemia cells. Exp. Cell Res. 196, 216-225.
49. Martelli A.M., Falcieri E., Gobbi P., Manzoli L., Cataldi A. Rana R.A. and Cocco L. (1992). Further considerations on the thermal stabilization of the nuclear matrix in mouse erythroleukemia cells. Cell Biol. Int. Rep. 16, 307-317.
50. Martelli A.M., Cocco L., Reiderer B.M. and Neri L.M. (1996). The nuclear matrix: a critical appraisal. Histol. Histopathol. 11, 1035-1048.
51. Martelli A.M., Bareggi R., Bortul R., Grill V., Narducci P. and Zweyer M. (1997). The nuclear matrix and apoptosis. Histochem. Cell Biol. 108, 1-10.
52. Martelli A.M., Bortul R., Fackelmayer F., Tazzari P.L., Bareggi R., Narducci P. and Zweyer M. (1999a). Biochemical and morphological characterization of the nuclear matrix from apoptotic HL60 cells. J. Cell. Biochem. 72, 35-46.
53. Martelli A.M., Bortul R., Bareggi R., Grill V., Narducci P. and Zweyer M. (1999b). Biochemical and morphological changes in the nuclear matrix prepared from apoptotic HL-60 cells. Effect of different stabilizing procedures. J. Cell. Biochem. 74, 99-110.
54. Matera A.G. (1999). Nuclear bodies: multifaceted subdomains of the interchromatin space. Trend Cell Biol. 9, 302-309.
55. Mattern K.A., van Goethem R.E., de Jong L. and van Driel R. (1997). Major internal nuclear matrix proteins are common to different human cell types. J. Cell Biochem. 65, 42-52.
56. McConnell M., Whalen A.M., Smith D.E. and Fisher P.A. (1987). Heat shock-induced changes in the structural stability of proteinaceous karyoskeletal elements in vitro and morphological effects in situ. J. Cell Biol. 105, 1087-1098.
57. Menz K., Radomski N. and Jost E. (1996). INMP, a novel intranuclear matrix protein related to the family of intermediate filament-like proteins: molecular cloning and sequence. Biochim. Biophys. Acta 1309, 14-20.
58. Mintz P.J., Patterson S.D., Neuwald A.F., Spahr C.S. and Spector D.L. (1999). Purification and biochemical characterization of interchromatin granule clusters. EMBO J. 18, 4308-4320.
59. Mirkovitch J., Mirault M.-E. and Laemmli U.K. (1984). Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell 39, 223-232.
60. Nakayasu H. and Berezney R. (1991). Nuclear matrins: identification of the major nuclear matrix proteins. Proc. Natl. Acad. Sci. USA 88, 10312-10316.
61. Neri L.M., Santi S., Marugg R.A., Riederer B.M., Capitani S., Cataldi A. and Martelli A.M. (1994). In vitro heat exposure induces a redistribution of nuclear matrix proteins in K562 erythroleukemia cells. Exp. Cell Res. 213, 275-285.
62. Neri L.M., Reiderer B.M., Marugg R.A., Capitani S. and Martelli A.M. (1995). The effect of sodium tetrathionate stabilization on the distribution of three nuclear matrix proteins in human K562 erythroleukemia cells. Histochem. Cell Biol. 104, 29-36.
63. ++ revealed by confocal microscopy. Microsc. Res. Tech. 36, 179-187.
64. ++. J. Histochem. Cytochem. 45, 295-305.
65. Neri L.M., Fackelmayer F.O., Zweyer M., Kohwi-Shigematsu T. and Martelli A.M. (1997c). Subnuclear localization of S/MAR-binding proteins is differently affected by in vitro stabilization with heat or Cu2+. Chromosoma 106, 81-93.
66. Neri L.M., Bortul R., Zweyer M., Tabellini G., Borgatti P., Marchisio M., Bareggi R., Capitani S. and Martelli A.M. (1999). Influence of different metal ions on the ultrastructure, biochemical properties, and protein localization of the K562 cell nuclear matrix. J. Cell. Biochem. 73, 342-354.
67. Nickerson J.A. (2001). Experimental observations of a nuclear matrix. J. Cell Sci. 114, 463-474.
68. Nickerson J.A., Krockmalnic G., Wan K.M. and Penman S. (1997). The nuclear matrix revealed by eluting chromatin from a cross-linked nucleus. Proc. Natl. Acad. Sci. USA 94, 4446-4450
69. Pardoll D. M., Vogelstein B. and Coffey D.S. (1980). A fixed site of DNA replication in eucaryotic cells. Cell 19, 527-536.
70. Pederson T. (1998). Thinking about a nuclear matrix. J. Mol. Biol. 277, 147-159.
71. Pederson T. (2000). Half a century of "the nuclear matrix". Mol. Biol. Cell 11, 799-805.
72. Phair R.D. and Misteli T. (2000). High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609.
73. Philimonenko V.V., Flechon J.-E. and Hozak P. (2001). The nucleoskeleton: a permanent structure of cell nuclei regardless of their transcriptional activity. Exp. Cell Res. 264, 201-210.
74. Qumsiyeh M.B. (1999). Structure and function of the nucleus: anatomy and physiology of chromatin. Cell. Mol. Life Sci. 55, 1129-1140.
75. Robertson J.D., Orrenius S. and Zhivotovsky B. (2000). Review: nuclear events in apoptosis. J. Struct. Biol. 129, 346-358.
76. Saredi A., Howard L. and Compton D.A. (1996). NuMA assembles into an extensive filamentous structure when expressed in the cell cytoplasm. J. Cell Sci. 109, 619-630.
77. Shopland L.S. and Lawrence J.B. (2000). Seeking common ground in nuclear complexity. J. Cell Biol. 150, F1-F4.
78. Sleeman J.E. and Lamond A.I. (1999a). Newly assembled snRNPs associate with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway. Curr. Biol. 9, 1065-1074.
79. Sleeman J.E. and Lamond A.I. (1999b). Nuclear organization of pre-mRNA splicing patterns. Curr. Biol. 11, 372-377.
80. Sodja C., Brown D.L., Walker P.R. and Chaly N. (1998). Splenic T lymphocytes die preferentially during heat induced apoptosis: NuMA reorganization as a marker. J. Cell Sci. 111, 2305-2313.
81. Spector D.L. (1993). Macromolecular domains within the cell nucleus. Annu. Rev. Biochem. 9, 265-315.
82. Stuurman N., Meijne A.M.L., van der Pol A.J., de Jong L., van Driel R. and van Renswoude J. (1990). The nuclear matrix from cells of different origin. Evidence for a common set of matrix proteins. J. Biol. Chem. 265, 5460-5465.
83. Takahashi A., Alnemri E.S., Lazebnik Y.A., Fernandes-Alnemri R., Litwack G., Moir R.D., Goldman R.D., Poirier G.G., Kaufmann S.H. and Earnshaw W.C. (1996). Cleavage of lamin A by Mch 2 a but not CPP32: multiple interleukin-1β-converting enzyme-related proteases with distinct substrate recognition proteins are active in apoptosis. Proc. Natl. Acad. Sci. USA 93, 8395-8400.
84. Taimen P., Vilijamaa M. and Kallajoki M. (2000). Preferential expression of NuMA in the nuclei of proliferating cells. Exp. Cell Res. 256, 140-149.
85. Tan J., Wooley J.H. and LeStourgeon W.M. (2000). Nuclear-matrix like filaments and fibrogranular complexes form through the rearrangement of specific ribonucleoproteins. Mol. Biol. Cell 11, 1547-1554.
86. Wan K.M., Nickerson J.A., Krockmalnic G. and Penman S. (1999). The nuclear matrix prepared by amine modification. Proc. Natl. Acad. Sci. USA 96, 933-938.
87. Wei X., Somanathan S., Samarabandu J. and Berezney R. (1999). Three-dimensional visualization of transcription sites and their association with splicing factor-rich nuclear speckles. J. Cell Biol. 146, 543-548.
88. Zeng C. (2000). NuMA: a nuclear protein involved in mitotic centrosome function. Microsc. Res. Tech. 49, 467-477.
89. Zeng C., He D, and Brinkley B.R. (1994). Localization of NuMA protein isoforms in the nuclear matrix of mammalian cells. Cell. Motil. Cytoskeleton 29, 167-176.