Summary
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1.
Protein composition of neuronal nuclei was studied at two stages of brain maturation, i.e., before (embryonic day 16; E16) and after (postnatal day 10; P10) shortening of the nucleosomal repeat length. Glial nuclei were analyzed in parallel as a control.
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Total nuclear or HCl- and 5% perchloric acid (PCA)-soluble proteins were analyzed by different electrophoretic techniques.
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Our results show an increase in the concentration of histone H1° with differentiation, although the H1 class undergoes an overall decrease.
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The chromatin of mature neurons is also enriched in the ubiquinated form of histone H2A (A24), while the high-mobility group (HMG) proteins 1 and 2 seem to decrease slightly relative to core histones.
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5.
Both quantitative and qualitative differences in the abundance of nonhistone proteins relative to histones accompany neuronal terminal differentiation.
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References
Allan, J., J., Rau, D. C., Harborne, N., and Gould, H. (1984). Higher order structure in a short repeat length chromatin.J. Cell Biol. 981320–1327.
Banchev, T., Srebreva, J., Zlatanova, J., and Tsanev, R. (1988). Immunofluorescent localization of histone H1° in the nuclei of proliferating and differentiating Friend cells.Exp. Cell Res. 177 1–8.
Brown, I. R. (1978). Postnatal appearance of a short DNA repeat length in neurons of the cerebral cortex.Biochem. Biophys. Res. Commun. 84285–292.
Cestelli, A., Di Liegro, I., Castiglia, D., Gristina, R., Ferraro, D., Salemi, G., and Savettieri, G. (1987). Triiodothyronine-induced shortening of chromatin repeat length in neurons cultured in a chemically defined medium.J. Neurochem. 481053–1059.
Di Liegro, I., and Cestelli, A. (1990). The relative proportion of H1° and A24 is reversed in oligodendrocytes during rat brain development.Cell. Mol. Neurobiol. 10267–274.
Fais, D., Prusov, A. N., and Poliakov, V. Yu (1982). The lack of histone H1 in the peripheral chromatin of rat liver nuclei.Cell Biol. Int. Rep. 6433–441.
Fais, D., Prusov, A. N., and Poliakov, V. Yu (1989). The anchorosome, a special chromatin granule for the anchorage of the interphase chromosome to the nuclear envelope.Cell Biol. Int. Rep. 13747–758.
Finley, D., and Varshavsky, A. (1985). The ubiquitin system-functions and mechanisms.Trends Biochem. Sci. 10 343–347.
Giulotto, E., Knights, K., and Stark, G. R. (1987). Hamster cells with increased rates of DNA amplification, a new phenotype.Cell 48837–845.
Gjerset, R., Gorka, C., Hasthorpe, S., Lawrence, J. J., and Eisen, H. (1982). Developmental and hormonal regulation of protein H1° in rodents.Proc. Natl. Acad. Sci. USA 792333–2337.
Goodwin, G., and Bustin, M. (1988). The HMG proteins and their genes. InArchitecture of Eukaryotic Genes (G. Kahl, Ed.), VCH, Weinheim, pp. 187–205.
Greenwood, P. D., and Brown, I. R. (1982). Developmental changes in DNase I digestability and RNA template activity of neuronal nuclei relative to the postnatal appearance of a short DNA repeat length.Neurochem. Res. 7965–975.
Greenwood, P. D., Silver, J. C., and Brown, I. R. (1981). Analysis of histones associated with neuronal and glial nuclei exhibiting divergent DNA repeat lengths.J. Neurochem. 37498–505.
Hutchison, N., and Weintraub, H. (1985). Localization of DNase I-sensitive sequences to specific regions of interphase nuclei.Cell 43471–482.
Ivanov, T. R., and Brown, I. R. (1989). Genes expressed in cortical neurons—Chromatin conformation and DNase I hypersensitive sites.Neurochem. Res. 14129–137.
Jaeger, A. W., and Kuenzle, C. C. (1982). The chromatin repeat length of brain cortex and cerebellar neurones changes concomitant with terminal differentiation.EMBO J. 1 811–816.
Kohlstaedt, L. A., Sung, E. C., Fujishige, A., and Cole, R. D. (1987). Non-histone chromosomal protein HMG1 modulates the histone H1-induced condensation of DNA.J. Biol. Chem. 262524–526.
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 227680–685.
Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. (1951). Protein measurement with the Folin phenol reagent.J. Biol. Chem. 193265–275.
Moorman, A. F. M., de Boer, P. A. J., Charles, R., and Lamers, W. H. (1987). The histone H1°/H5 variant and terminal differentiation of cells during development ofXenopus laevis.Differentiation 35100–107.
Nachaeva, G. A., Guschin, D. Y., Preobrazhenskaya, O. V., Karpov, V. L., Ebralidse, K. K., and Mirzabekov, A. D. (1989). Change in the pattern of histone binding to DNA upon transcriptional activation.Cell 5827–36.
Pearson, E. C., Bates, D. L., Prospero, T. D., and Thomas, J. O. (1984). Neuronal nuclei and glial nuclei from mammalian cerebral cortex. Nucleosomal repeat lengths, DNA contents and H1 contents.Eur. J. Biochem. 144353–360.
Pehrson, J., and Cole, R. D. (1980). Histone H1° accumulates in growth inhibited cultured cells.Nature 28543–44.
Pehrson, J., and Cole, R. D. (1982). Histone H1 subfractions and H1° turnover at different rates in non-dividing cells.Biochemistry 21456–460.
Pina, B., and Suau, P. (1987a). Changes in the proportions of histone H1° subtypes in brain cortical neurons.FEBS Lett. 210161–164.
Pina, B., and Suau, P. (1987b). Changes in Histone H2A and H3 variant composition in differentiating and mature rat cortical neurons.Dev. Biol. 12351–58.
Pina, B., Martinez, P., Simon, L., and Suau, P. (1984). Differential kinetics of histone H1° accumulation in neuronal and glial cells from rat cerebral cortex during postnatal development.Biochem. Biophys. Res. Commun. 123697–702.
Pina, B., Martinez, P., and Suau, P. (1987). Changes in H1 complement in differentiating rat-brain cortical neurons.Eur. J. Biochem. 16471–76.
Roche, J., Gorka, C., Goeltz, P., and Lawrence, J. J. (1985). Association of histone H1° with a gene repressed during liver development.Nature 314197–198.
Schlissel, M. S., and Brown, D. D. (1984). The transcriptional regulation of Xenopus 5S RNA genes in chromatin: The roles of active stable transcription complexes and histone H1.Cell 37903–913.
Thoma, F. (1988). The role of histone H1 in nucleosomes and chromatin fibers. InArchitecture of Eukaryotic Genes (G. Kahl, Ed.), VCH, Weinheim, pp. 163–185.
Thomas, J. O., and Thompson, R. J. (1977). Variation in chromatin structure in two cell types from the same tissue: A short DNA repeat length in cerebral cortex neurons.Cell 10633–640.
Weintraub, H. (1984). Histone-H1-dependent chromatin superstructures and the suppression of gene activity.Cell 3817–27.
Weintraub, H., and Groudine, M. (1976). Chromosomal subunits in active genes have an altered conformation.Nature 193848–856.
Wolffe, A. P., and Brown, D. D. (1988). Developmental regulation of two 5S ribosomal RNA genes.Science 2411626–1632.
Zlatanova, J. (1990). Histone H1 and the regulation of transcription of eukaryotic genes.Trends Biochem. Sci. 15273–276.
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Cestelli, A., Castiglia, D., Di Liegro, C. et al. Qualitative differences in nuclear proteins correlate with neuronal terminal differentiation. Cell Mol Neurobiol 12, 33–43 (1992). https://doi.org/10.1007/BF00711637
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DOI: https://doi.org/10.1007/BF00711637