The novel SAR-binding domain of scaffold attachment factor A (SAF-A) is a target in apoptotic nuclear breakdown

EMBO Journal

Volumn 16, Issue 24, 1997, Pages 7361-7371

  Göhring, Frank ^a   Schwab, Birgit L ^a   Nicotera, Pierluigi ^a   Leist, Marcel ^a   Fackelmayer, Frank O ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA BINDING PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; NUCLEAR PROTEIN; RNA;

APOPTOSIS; ARTICLE; BINDING SITE; CELL DEATH; CHROMATIN; CHROMATIN STRUCTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN DOMAIN; RNA METABOLISM;

AMINO ACID SEQUENCE; APOPTOSIS; BINDING SITES; CLONING, MOLECULAR; DNA, BACTERIAL; DNA-BINDING PROTEINS; ESCHERICHIA COLI; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN U; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; JURKAT CELLS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NECROSIS; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; RECOMBINANT FUSION PROTEINS; RIBONUCLEOPROTEINS; RNA, HETEROGENEOUS NUCLEAR;

EID: 0041177008     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.24.7361     Document Type: Article

References (67)

1. Adachi, Y., Käs, E. and Laemmli, U.K. (1989) Preferential, cooperative binding of DNA topoisomerase II to scaffold-associated regions. EMBO J., 8, 3997-4006.
2. Adam, S.A., Marr, R.S. and Gerace, L. (1990) Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol., 111, 807-816.
3. 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.
4. Berezney, R., Mortillaro, M.J., Ma, H., Wei, X. and Samarabandu, J. (1995) The nuclear matrix: a structural milieu for genomic function. Int. Rev. Cytol., 162A, 1-65.
5. Bode, J., Stengert-Iber, M., Kay, V., Schlake, T. and Dietz-Pfeilstetter, A. (1996) Scaffold/matrix-attached regions: topological switches with multiple regulatory functions. Crit. Rev. Eukaryot. Gene Expr., 6, 115-138.
6. Boy de la Tour, E. and Laemmli, U.K. (1988) The metaphase scaffold is helically folded: sister chromatids have predominantly opposite helical handedness. Cell, 55, 937-944.
7. Choi, Y.D. and Dreyfuss, G. (1984) Isolation of the heterogeneous nuclear RNA-ribonucleoprotein complex (hnRNP): a unique supramolecular assembly. Proc. Natl Acad. Sci. USA, 81, 7471-7475.
8. Cockerill, P.N. and Garrard, W.T. (1986) Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell, 44, 273-282.
9. Cohen, G.M., Sun, X.M. Snowden, R.T., Dinsdale, D. and Skilleter, D.N. (1992) Key morphological features of apoptosis may occur in the absence of internucleosomal DNA fragmentation. Biochem. J., 286, 331-334.
10. Dickinson, L.A. and Kohwi-Shigematsu, T. (1995) Nucleolin is a matrix attachment region DNA-binding protein that specifically recognizes a region with high base-impairing potential. Mol. Cell. Biol., 15, 456-165.
11. Dickinson, L.A., Joh, T., Kohwi, Y. and Kohwi-Shigematsu, T. (1992) A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell, 70, 631-645.
12. Dreyfuss, G., Choi, Y.D. and Adam, S.A. (1984) Characterization of heterogeneous nuclear RNA-protein complexes in vivo with monoclonal antibodies. Mol. Cell. Biol., 4, 1104-1114.
13. Dreyfuss, G., Matunis, M.J., Pinol-Roma, S. and Burd, C.G. (1993) hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Rev. Biochem., 62, 289-321.
14. Fackelmayer, F.O. and Richter, A. (1994) Purification of two isoforms of hnRNP-U and characterization of their nucleic acid binding activity. Biochemistry, 33, 10416-10422.
15. Fackelmayer, F.O., Dahm, K., Renz, A., Ramsperger, U. and Richter, A. (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.
16. Fey, E.G., Krochmalnic, G. and Penman, S. (1986) The nonchromatin substructures of the nucleus: the ribonucleoprotein (RNP)-containing and RNP-depleted matrices analyzed by sequential fractionation and resinless section electron microscopy. J. Cell Biol., 102, 1654-1665.
17. Filipski, J., Leblanc, J., Youdale, T., Sikorska, M. and Walker, P.R. (1990) Periodicity of DNA folding in higher order chromatin structures. EMBO J., 9, 1319-1327.
18. Garrard, W.T. (1990) Chromosomal loop organization in eukaryotic genomes. In Eckstein, F. and Lilley, D.J.M. (eds), Nucleic Acids and Molecular Biology. Springer-Verlag, Heidelberg, pp. 163-176.
19. Gasser, S.M. and Laemmli, U.K. (1986) Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D.melanogaster. Cell, 46, 521-530.
20. Gasser, S.M. and Laemmli, U.K. (1987) A glimpse at chromosomal order. Trends Genet., 3, 16-22.
21. Göhring, F. and Fackelmayer, F.O. (1997) The scaffold/matrix attachment region binding protein hnRNP-U (SAF-A) is directly bound to chromosomal DNA in vivo: a chemical cross-linking study. Biochemistry, 36, 8276-8283.
22. Hancock, R. (1974) Interphase chromosomal deoxyribonucleoprotein isolated as a discrete structure from cultured cells. J. Mol. Biol., 86, 649-663.
23. Harlow, E. and Lane, D.P (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. He, D.C., Nickerson, J.A. and Penman, S. (1990) Core filaments of the nuclear matrix. J. Cell Biol., 110, 569-580.
25. Hsu, H.L. and Yeh, N.H. (1996) Dynamic changes of NuMA during the cell cycle and possible appearance of a truncated form of NuMA during apoptosis. J. Cell Sci., 109, 277-288.
26. Izaurralde, E., Käs, E. and Laemmli, U.K. (1989) Highly preferential nucleation of histone H1 assembly on scaffold-associated regions. J. Mol. Biol., 210, 573-585.
27. Jenuwein, T., Forrester, W.C., Fernandez-Herrero, L.A., Laible, G., Dull, M. and Grosschedl, R. (1997) Extension of chromatin accessibility by nuclear matrix attachment regions. Nature, 385, 269-272.
28. Käs, E. and Laemmli, U.K. (1992) In vivo topoisomerase II cleavage of the Drosophila histone and satellite III repeats: DNA sequence and structural characteristics. EMBO J., 11, 705-716.
29. Kiledjian, M. and Dreyfuss, G. (1992) Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J., 11, 2655-2664.
30. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
31. Laemmli, U.K., Käs, E., Poljak, L. and Adachi, Y. (1992) Scaffold-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr. Opin. Genet. Dev., 2, 275-285.
32. LaFond, R.E., Woodcock, H., Woodcock, C.L., Kundahl, E.R. and Lucas, J.J. (1983) Generation of an internal matrix in mature avian erythrocyte nuclei during reactivation in cytoplasts. J. Cell Biol., 96, 1815-1819.
33. Lazebnik, Y.A., Takahashi, A., Poirier, G.G., Kaufmann, S.H. and Earnshaw, W.C. (1995) Characterization of the execution phase of apoptosis in vitro using extracts from condemned-phase cells. J. Cell Sci., Suppl. 19, 41-49.
34. Leist, M., Single, B., Castoldi, A.F., Kuhnle, S. and Nicotera, P. (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med., 185, 1481-1486.
35. Lichter, P., Cremer, T., Borden, J., Munuelidis, L. and Ward, D.C. (1988) Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum. Genet., 80, 224-234.
36. Löwenadler, B. et al. (1987) A gene fusion system for generating antibodies against short peptides. Gene, 58, 87-97.
37. Luderus, M.E., de Graaf, A., Mattia, E., den Blaauwen, J.L., Grande, M.A., de Jong, L. and van Driel, R. (1992) Binding of matrix attachment regions to lamin B1. Cell, 70, 949-959.
38. Marshall, W.F., Dernburg, A.F., Harmon, B., Agard, D.A. and Sedat, J.W. (1996) Specific interactions of chromatin with the nuclear envelope: positional determination within the nucleus in Drosophila melanogaster. Mol. Biol. Cell, 7, 825-842.
39. Matiba, B., Mariani, S.M. and Krammer, P.H. (1997) The CD95 system and the death of a lymphocyte. Semin. Immunol., 9, 59-68.
40. Mattern, K.A., Humbel, B.M., Muijsers, A.O., De Jong, L. and Van Driel, R. (1996) hnRNP proteins and B23 are the major proteins of the internal nuclear matrix of HeLa S3 cells. J. Cell. Biochem., 62, 275-289.
41. 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.
42. 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.
43. Nakajima, T., Morita, K., Ohi, N., Arai, T. Nozaki, N., Kikuchi, A., Osaka, F., Yamao, F. and Oda, K. (1996) Degradation of topoisomerase IIalpha during adenovirus E1A-induced apoptosis is mediated by the activation of the ubiquitin proteolysis system. J. Biol. Chem., 271, 24842-24849.
44. Nickerson, J.A., Blencowe, B.J. and Penman, S. (1995) The architectural organization of nuclear metabolism. Int. Rev. Cytol., 162A, 67-123.
45. Renz, A. and Fackelmayer, F.O. (1996) Purification and molecular cloning of the scaffold attachment factor B (SAF-B), a novel human nuclear protein that specifically binds to S/MAR-DNA. Nucleic Acids Res., 24, 843-849.
46. Romig, H., Fackelmayer, F.O., Renz, A., Ramsperger, U. and Richter, A. (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 J., 11, 3431-3440.
47. Romia, H., Ruff, J., Fackelmayer, F.O., Patil, M.S. and Richter, A. (1994) Characterisation of two intronic nuclear-matrix-attachment regions in the human DNA topoisomerase I gene. Eur. J. Biochem., 221, 411-419.
48. Rost, B. (1996) PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol., 266, 525-339.
49. Saitoh, Y. and Laemmli, U.K. (1994) Metaphase chromosome structure: bands arise from a differential folding path of the highly AT-rich scaffold. Cell, 76, 609-622.
50. Sambrook, J., Maniatis, T. and Fritsch, E.F. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
51. Stief, A., Winter, D.M., Strätling, W.H. and Sippel, A.E. (1989) A nuclear DNA attachment element mediates elevated and position-independent gene activity. Nature, 341, 343-345.
52. Strick, R. and Laemmli, U.K. (1995) SARs are cis DNA elements of chromosome dynamics: synthesis of a SAR repressor protein. Cell, 83, 1137-1148.
53. Sun, X.M., Snowden, R.T., Dinsdale, D., Ormerod, M.G. and Cohen, G.M. (1994) Changes in nuclear chromatin precede internucleosomal DNA cleavage in the induction of apoptosis by etoposide. Biochem. Pharmacol., 47, 187-195.
54. Surdej, P., Got, C., Rosset, R. and Miassod, R. (1990) Supragenic loop organization: mapping in Drosophila embryos, of scaffold-associated regions on a 800 kilobase DNA continuum cloned from the 14B-15B first chromosome region. Nucleic Acids Res., 18, 3713-3722.
55. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA, 76, 4350-4354.
56. Tsutsui, K., Tsutsui, K., Okada, S., Watarai, S., Seki, S., Yasuda, T. and Shohmori, T. (1993) Identification and characterization of a nuclear scaffold protein that binds the matrix attachment region DNA. J. Biol. Chem., 268, 12886-12894.
57. Vogelstein, B., Pardoll, D.M. and Coffey, D.S. (1980) Supercoiled loops and eucaryotic DNA replicaton. Cell, 22, 79-85.
58. von Kries, J.P., Buck, F. and Strätling, W.H. (1994) Chicken MAR binding protein p120 is identical to human heterogeneous nuclear ribonucleoprotein (hnRNP) U. Nucleic Acids Res., 22, 1215-1220.
59. Waterhouse, N. et al. (1996) Heteronuclear ribonucleoproteins C1 and C2, components of the spliceosome, are specific targets of interleukin 1beta-converting enzyme-like proteases in apoptosis. J. Biol. Chem., 271, 29335-29341.
60. Weaver, V.M., Carson, C.E., Walker, P.R., Chaly, N., Lach, B., Raymond, Y., Brown, D.L. and Sikorska, M. (1996) Degradation of nuclear matrix and DNA cleavage in apoptotic thymocytes. J. Cell Sci., 109, 45-56.
61. Weis, M., Schlegel, J., Kass, G.E., Holmstrom, T.H., Peters, I., Eriksson, J., Orrenius, S. and Chow, S.C. (1995) Cellular events in Fas/APO-1-mediated apoptosis in JURKAT T lymphocytes. Exp. Cell Res., 219, 699-708.
62. Wessel, D. and Flügge, U.I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem., 138, 141-143.
63. Xing, Y., Johnson, C.V., Dobner, P.R. and Lawrence, J.B. (1993) Higher level organization of individual gene transcription and RNA splicing. Science, 259, 1326-1330.
64. Yanagisawa, J., Ando, J., Nakayama, J., Kohwi, Y. and Kohwi-Shigematsu, T. (1996) A matrix attachment region (MAR)-binding activity due to a p114 kilodalton protein is found only in human breast carcinomas and not in normal and benign breast disease tissues. Cancer Res., 56, 457-462.
65. Zhao, K., Käs, E., Gonzalez, E. and Laemmli, U.K. (1993) SAR-dependent mobilization of histone H1 by HMG-I/Y in vitro: HMG-I/Y is enriched in H1-depleted chromatin. EMBO J., 12, 3237-3247.
66. Zuckerkandl, E. and Villet, R. (1988) Generation of high specificity of effect through low-specificity binding of proteins to DNA. FEBS Lett., 231, 291-298.
67. Zweyer, M., Riederer, B.M., Ochs, R.L., Fackelmayer, F.O., Kohwi-Shigematsu, T., Bareggi, R., Narducci, P. and Martelli, A.M. (1997) Association of nuclear matrix proteins with granular and threaded nuclear bodies in cell lines undergoing apoptosis. Exp. Cell Res., 230, 325-336.