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Research Article

Nucleolin Is a Matrix Attachment Region DNA-Binding Protein That Specifically Recognizes a Region with High Base-Unpairing Potential

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Pages 456-465 | Received 08 Apr 1994, Accepted 26 Sep 1994, Published online: 30 Mar 2023

REFERENCES

  • Adachi, Y., E. Käs, and U. K. Laemmli. 1989. Preferential, cooperative binding of DNA topoisomerase II to scaffold-associated regions. EMBO J. 8:3997–4006.
  • Barrijal, S., M. Perros, Z. Gu, B. L. Avalosse, P. Belenguer, F. Amalric, and J. Rommelaere. 1992. Nucleolin forms a specific complex with a fragment of the viral (minus) strand of minute virus of mice DNA. Nucleic Acids Res. 20: 5053–5060.
  • Belenguer, P., M. Caizergues-Ferrer, J.-C. Labbé, M. Dorée, and F. Amalric. 1990. Mitosis-specific phosphorylation of nucleolin by p34cdc2 protein kinase. Mol. Cell. Biol. 10:3607–3618.
  • Berrios, M., N. Osheroff, and P. A. Fisher. 1985. In situ localization of DNA topoisomerase II, a major polypeptide component of the Drosophila nuclear matrix fraction. Proc. Natl. Acad. Sci. USA 82:4142–4146.
  • Bidwell, J. P., A. J. van Wijnen, E. G. Fey, S. Dworetzky, S. Penman, J. L. Stein, J. B. Lian, and G. S. Stein. 1993. Osteocalcin gene promoter-binding factors are tissue-specific nuclear matrix components. Proc. Natl. Acad. Sci. USA 90:3162–3166.
  • Bode, J., Y. Kohwi, L. Dickinson, T. Joh, D. Klehr, C. Mielke, and T. Kohwi-Shigematsu. 1992. Biological significance of unwinding capability of nuclear matrix-associating DNAs. Science 255:195–197.
  • Bode, J., and K. Maass. 1988. Chromatin domain surrounding the human interferon-β gene as defined by scaffold-attached regions. Biochemistry 27: 4706–4711.
  • Bolla, R. I., D. C. Braaten, Y. Shiomi, M. B. Hebert, and D. Schlessinger. 1985. Localization of specific rDNA spacer sequences to the mouse L-cell nucleolar matrix. Mol. Cell. Biol. 5:1287–1294.
  • Borer, R. A., C. F. Lehner, H. M. Eppenberger, and E. A. Nigg. 1989. Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56:379–390.
  • Bouche, G., M. Caizergues-Ferrer, B. Bugler, and F. Amalric. 1984. Interrelations between the maturation of a 100 kDa nucleolar protein and pre-rRNA synthesis in CHO cells. Nucleic Acids Res. 12:3025–3035.
  • Bugler, B., M. Caizergues-Ferrer, G. Bouche, H. Bourbon, and F. Amalric. 1982. Detection and localization of a class of proteins immunologically related to a 100-kDa nucleolar protein. Eur. J. Biochem. 128:475–480.
  • Caizergues-Ferrer, M., P. Mariottini, C. Curie, B. Lapeyre, N. Gas, F. Amalric, and F. Amaldi. 1989. Nucleolin from Xenopus laevis: cDNA cloning and expression during development. Genes Dev. 3:324–333.
  • Chen, C.-M., S.-Y. Chiang, and N.-H. Yeh. 1991. Increased stability of nucleolin in proliferating cells by inhibition of its self-cleaving activity. J. Biol. Chem. 266:7754–7758.
  • Cockell, M., S. Frutiger, G. J. Hughes, and S. M. Gasser. 1994. The yeast protein encoded by PUB1 binds T-rich single stranded DNA. Nucleic Acids Res. 22:32–40.
  • Cockerill, P. N., and W. T. Garrard. 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.
  • Cockerill, P. N., M.-H. Yuen, and W. T. Garrard. 1987. The enhancer of the immunoglobulin heavy chain locus is flanked by presumptive chromosomal loop anchorage elements. J. Biol. Chem. 262:5394–5397.
  • Cunningham, J. M., M. E. Purucker, S. M. Jane, B. Safer, E. F. Vanin, P. A. Ney, C. H. Lowrey, and A. W. Nienhuis. 1994. The regulatory element 39 to the Aγ-globin gene binds to the nuclear matrix and interacts with special A-T-rich binding protein 1 (SATB1), an SAR/MAR-associating region DNA binding protein. Blood 84:1298–1308.
  • de Lange, T. 1992. Human telomeres are attached to the nuclear matrix. EMBO J. 11:717–724.
  • 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.
  • Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475–1489.
  • Dijkwel, P. A., and J. C. Hamlin. 1988. Matrix attachment regions are positioned near replication initiation sites, genes, and an interamplicon junction in the amplified dihydrofolate reductase domain of Chinese hamster ovary cells. Mol. Cell. Biol. 8:5398–5409.
  • Earnshaw, W. C. 1988. Mitotic chromosome structure. Bioessays 9:147–150.
  • Earnshaw, W. C., and M. S. Heck. 1985. Localization of topoisomerase II in mitotic chromosomes. J. Cell Biol. 100:1716–1725.
  • 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.
  • Franke, W. W., J. A. Kleinschmidt, H. Spring, G. Krohne, C. Grund, M. F. Trendelenburg, M. Stoehr, and U. Scheer. 1981. A nucleolar skeleton of protein filaments demonstrated in amplified nucleoli of Xenopus laevis. J. Cell Biol. 90:289–299.
  • Fried, M., and D. M. Crothers. 1981. Equilibria and kinetics of lac repressor-operator interaction by polyacrylamide gel electrophoresis. Nucleic Acids Res. 9:6505–6525.
  • Gasser, S. M., and U. K. Laemmli. 1986. Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D. melanogaster. Cell 46:521–530.
  • Gasser, S. M., and U. K. Laemmli. 1986. The organization of chromatin loops: characterization of scaffold sttachment sites. EMBO J. 5:511–518.
  • Gasser, S. M., and U. K. Laemmli. 1987. A glimpse at chromosomal order. Trends Genet. 3:16–22.
  • Gasser, S. M., T. Laroche, J. Falquet, E. Boy de la Tour, and U. K. Laemmli. 1986. Metaphase chromosome structure. Involvement of topoisomerase II. J. Mol. Biol. 188:613–629.
  • Ghisolfi, L., G. Joseph, F. Amalric, and M. Erard. 1992. The glycine-rich domain of nucleolin has an unusual supersecondary structure responsible for its RNA-helix-destabilizing properties. J. Biol. Chem. 267:2955–2959.
  • Hager, D. A., and R. R. Burgess. 1980. Elution of proteins from sodium dodecyl sulfate-polyacrylamide gels, removal of sodium dodecyl sulfate, and renaturation of enzymatic activity: results with sigma subunit of Escherichia coli RNA polymerase, wheat germ DNA topoisomerase, and other enzymes. Anal. Biochem. 109:76–86.
  • Hakes, D. J., and R. Berezney. 1991. DNA binding properties of the nuclear matrix and individual nuclear matrix proteins. Evidence for salt-resistant DNA binding sites. J. Biol. Chem. 266:11131–11140.
  • Herrera, A. H., and M. O. J. Olson. 1986. Association of protein C23 with rapidly labeled nucleolar RNA. Biochemistry 25:6258–6264.
  • Hozak, P., A. B. Hassan, D. A. Jackson, and P. R. Cook. 1993. Visualization of replication factories attached to a nucleoskeleton. Cell 73:361–373.
  • Ishikawa, F., M. J. Matunis, G. Dreyfuss, and T. R. Cech. 1993. Nuclear proteins that bind the pre-mRNA 39 splice site sequence r(UUAG/G) and the human telomeric DNA sequence d(TTAGGG)n Mol. Cell. Biol. 13: 4301–4310.
  • Izaurralde, E., E. Käs, and U. Laemmli. 1989. Highly preferential nucleation of histone H1 assembly on scaffold-associated regions. J. Mol. Biol. 210:573–585.
  • Jackson, D. A., and P. R. Cook. 1986. Replication occurs at a nucleoskeleton. EMBO J. 5:1403–1410.
  • Jackson, D. A., P. R. Cook, and S. B. Patel. 1984. Attachment of repeated sequences to the nuclear cage. Nucleic Acids Res. 12:6709–6726.
  • Jarman, A. P., and D. R. Higgs. 1988. Nuclear scaffold attachment sites in the human globin gene complexes. EMBO J. 7:3337–3344.
  • Jordan, G. 1987. At the heart of the nucleolus. Nature (London) 329:489–490.
  • Kadonaga, J. T., and R. Tjian. 1986. Affinity purification of sequence-specific DNA binding proteins. Proc. Natl. Acad. Sci. USA 83:5889–5893.
  • Kaufmann, S. H., W. Gibson, and J. H. Shaper. 1983. Characterization of the major polypeptides of the rat liver nuclear envelope. J. Biol. Chem. 258: 2710–2719.
  • Kim, C., R. O. Snyder, and M. S. Wold. 1992. Binding properties of replication protein A from human and yeast cells. Mol. Cell. Biol. 12:3050–3059.
  • Klehr, D., K. Maass, and J. Bode. 1991. Scaffold-attached regions from the human interferon-β domain can be used to enhance the stable expression of genes under the control of various promoters. Biochemistry 30:1264–1270.
  • Kohwi-Shigematsu, T., and Y. Kohwi. 1990. Torsional stress stabilizes extended base unpairing in suppressor sites flanking immunoglobulin heavy chain enhancer. Biochemistry 29:9551–9560.
  • Kopka, M. L., C. Yoon, D. Goodsell, P. Pjura, and R. E. Dickerson. 1985. The molecular origin of DNA-drug specificity in netropsin and distamycin. Proc. Natl. Acad. Sci. USA 82:1376–1380.
  • Koudelka, G. B., S. C. Harrison, and M. Ptashne. 1987. Effect of noncon-tacted bases on the affinity of 434 operator for 434 repressor and Cro. Nature (London) 326:886–888.
  • Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680–685.
  • Levi-Wilson, B., and C. Fortier. 1990. The limits of the DNase I-sensitive domain of the human apolipoprotein β gene coincide with the locations of the chromosomal anchorage loops and define the 59 and 39 boundaries of the gene. J. Biol. Chem. 264:21196–21204.
  • Long, B. H., and R. L. Ochs. 1983. Nuclear matrix, hnRNA, and snRNA in Friend erythroleukemia nuclei depleted of chromatin by low ionic strength EDTA. Biol. Cell 48(2–3):89–98.
  • 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.
  • McKnight, R. A., A. Shamay, L. Sankaran, R. J. Wall, and L. Hennighausen. 1992. Matrix-attachment regions can impart position-independent regulation of a tissue-specific gene in transgenic mice. Proc. Natl. Acad. Sci. USA 89: 6943–6947.
  • Mielke, C., Y. Kohwi, T. Kohwi-Shigematsu, and J. Bode. 1990. Hierarchical binding of DNA fragments derived from scaffold-attached regions: correlation of properties in vitro and function in vivo. Biochemistry 29:7475–7485.
  • Mirkovitch, J., M.-E. Mirault, and U. K. Laemmli. 1984. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell 39:223–232.
  • Nakagomi, K., Y. Kohwi, L. A. Dickinson, and T. Kohwi-Shigematsu. 1994. A novel DNA-binding motif in the nuclear matrix attachment DNA-binding protein SATB1. Mol. Cell. Biol. 14:1852–1860.
  • Nelson, W. G., K. J. Pienta, E. R. Barrack, and D. S. Coffey. 1986. The role of the nuclear matrix in the organization and function of DNA. Annu. Rev. Biophys. Biophys. Chem. 15:457–475.
  • Olson, M. Personal communication.
  • Olson, M. O. J., Z. M. Rivers, B. A. Thompson, W.-Y. Kao, and S. T. Case. 1983. Interaction of nucleolar phosphoprotein C23 with cloned segments of rat ribosomal deoxyribonucleic acid. Biochemistry 22:3345–3351.
  • Olson, M. O. J., and B. A. Thompson. 1983. Distributions of proteins among chromatin components of nucleoli. Biochemistry 22:3187–3193.
  • Olson, M. O. J., M. O. Wallace, A. H. Herrera, L. Marshall-Carlson, and R. C. Hunt. 1986. Preribosomal ribonucleoprotein particles are a major component of a nucleolar matrix fraction. Biochemistry 25:484–491.
  • Pfeifle, J., J. M. Wolff, and F. A. Anderer. 1987. Quantitation and potential function of nucleolar phosphoprotein pp105 in mouse tumor cells, embryonic cells and normal tissues. Comp. Biochem. Physiol. 87B:309–312.
  • Phi-Van, L., and W. H. Strätling. 1988. The matrix attachment regions of the chicken lysozyme gene co-map with the boundaries of the chromatin domain. EMBO J. 7:655–664.
  • Phi-Van, L., and W. H. Strätling. 1990. Association of DNA with nuclear matrix. Prog. Mol. Subcell. Biol. 11:1–11.
  • Phi-Van, L., J. P. von Kries, W. Ostertag, and W. H. Strätling. 1990. The chicken lysozyme 59 matrix attachment region increases transcription from a heterologous promoter in heterologous cells and dampens position effects on the expression of transfected genes. Mol. Cell. Biol. 10:2302–2307.
  • Razin, S. V., M. G. Kekelidge, E. M. Lukanidin, K. Scherrer, and G. P. Georgiev. 1986. Replication origins are attached to the nuclear skeleton. Nucleic Acids Res. 14:8189–8207.
  • 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 J. 11:3431–3440.
  • Sapp, M., R. Knippers, and A. Richter. 1986. DNA binding properties of a 110 kDa nucleolar protein. Nucleic Acids Res. 14:6803–6820.
  • Schmidt, A. M., S. U. Herterich, and G. Krauss. 1991. A single-stranded DNA binding protein from S. cerevisiae specifically recognizes the T-rich strand of the core sequence of ARS elements and discriminates against mutant sequences. EMBO J. 10:981–985.
  • Shiomi, Y., J. Powers, R. I. Bolla, T. V. Nguyen, and D. Schlessinger. 1986. Proteins and RNA in mouse L-cell core nucleoli and nucleolar matrix. Biochemistry 25:5747–5751.
  • Smith, H. C., and R. Berezney. 1980. DNA polymerase alpha is tightly bound to the nuclear matrix of actively replicating liver. Biochem. Biophys. Res. Commun. 97:1541–1547.
  • Smith, H. C., and L. I. Rothblum. 1987. Ribosomal DNA sequences attached to the nuclear matrix. Biochem. Genet. 25:863–879.
  • Sperry, A. O., V. C. Blasquez, and W. T. Garrard. 1989. Dysfunction of chromosomal loop attachment sites: illegitimate recombination linked to matrix association regions and topoisomerase II. Proc. Natl. Acad. Sci. USA 86:5497–5501.
  • Srivastava, M., P. J. Fleming, H. B. Pollard, and A. L. Burns. 1989. Cloning and sequencing of the human nucleolin cDNA. FEBS Lett. 250:99–105.
  • Stief, A., D. M. Winter, W. H. Stratling, and A. E. Sippel. 1989. A nuclear DNA attachment element mediates elevated and position-independent gene activity. Nature (London) 341:343–345.
  • Theunissen, O., F. Rudt, U. Guddat, H. Mentzel, and T. Pieler. 1992. RNA and DNA binding zinc fingers in Xenopus TFIIIA. Cell 71:679–690.
  • Tsutsui, K., and K. Tsutsui. Personal communication.
  • 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.
  • Vaughn, J. P., P. A. Dijkwel, L. H. F. Mullenders, and J. L. Hamlin. 1990. Replication forks are associated with the nuclear matrix. Nucleic Acids Res. 18:1965–1969.
  • von Kries, J. P., F. Buck, and W. H. Strätling. 1994. Chicken MAR binding protein p120 is identical to human heterogeneous nuclear ribonucleoprotein (hnRNP) U. Nucleic Acids Res. 22:1215–1220.
  • von Kries, J. P., H. Buhrmester, and W. H. Strätling. 1991. A matrix/scaffold attachment region binding protein: identification, purification, and mode of binding. Cell 64:123–135.
  • Xing, Y., C. V. Johnson, P. R. Dobner, and J. B. Lawrence. 1993. Higher level organization of individual gene transcription and RNA splicing. Science 259:1326–1330.
  • Yang-Yen, H.-F., and L. I. Rothblum. 1986. Partial nucleotide sequence of a 3.4 kb fragment from the rat ribosomal DNA nontranscribed spacer. Nucleic Acids Res. 14:5557–5557.
  • Zhao, K., E. Käs, E. Gonzales, and U. K. Laemmli. 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.

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