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. 1986 Aug 26;14(16):6507–6523. doi: 10.1093/nar/14.16.6507

Chicken histone genes retain nuclear matrix association throughout the cell cycle.

S Dalton, H B Younghusband, J R Wells
PMCID: PMC311660  PMID: 2428014

Abstract

The association between histone genes and the nuclear matrix (NM) during periods of high (S-phase) and low (non-S-phase) transcriptional activity has been investigated with synchronized cells from a chicken erythroid cell line (abbreviated ts34). By DNase I and restriction enzyme analysis, these studies reveal that both core and linker histone genes (represented by H2A and H1 genes respectively) are attached to the NM independent of their transcriptional activity during the cell-cycle. The tissue-specific histone gene H5, expressed constitutively, is nuclear matrix (NM)-associated in ts34 cells but is found in the supernatant (S/N) fractions of a non-erythroid T-cell line. Furthermore, we show that DNA sequences necessary for NM-attachment of the H5 gene lie within a 780 base pair region spanning part of the coding and 5' non-translated region. Of the three non-histone genes investigated, beta-actin sequences are expressed and are NM-attached, feather keratin genes are not expressed and predominate in the S/N, and beta-globin genes although not expressed in the ts34 cell line used were found in the NM fraction. In this case the association may be fortuitous or may reflect an early event prior to transcription of globin genes in differentiating erythroid cells. These results generally support the notion that actively transcribed genes are NM-attached, but that attachment per se is not synonymous with transcription.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adolph K. W., Cheng S. M., Laemmli U. K. Role of nonhistone proteins in metaphase chromosome structure. Cell. 1977 Nov;12(3):805–816. doi: 10.1016/0092-8674(77)90279-3. [DOI] [PubMed] [Google Scholar]
  2. Bellard M., Gannon F., Chambon P. Nucleosome structure III: the structure and transcriptional activity of the chromatin containing the ovalbumin and globin genes in chick oviduct nuclei. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):779–791. doi: 10.1101/sqb.1978.042.01.078. [DOI] [PubMed] [Google Scholar]
  3. Benyajati C., Worcel A. Isolation, characterization, and structure of the folded interphase genome of Drosophila melanogaster. Cell. 1976 Nov;9(3):393–407. doi: 10.1016/0092-8674(76)90084-2. [DOI] [PubMed] [Google Scholar]
  4. Berezney R., Buchholtz L. A. Dynamic association of replicating DNA fragments with the nuclear matrix of regenerating liver. Exp Cell Res. 1981 Mar;132(1):1–13. doi: 10.1016/0014-4827(81)90076-8. [DOI] [PubMed] [Google Scholar]
  5. Beug H., Doederlein G., Freudenstein C., Graf T. Erythroblast cell lines transformed by a temperature-sensitive mutant of avian erythroblastosis virus: a model system to study erythroid differentiation in vitro. J Cell Physiol Suppl. 1982;1:195–207. doi: 10.1002/jcp.1041130427. [DOI] [PubMed] [Google Scholar]
  6. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bloom K. S., Anderson J. N. Fractionation of hen oviduct chromatin into transcriptionally active and inactive regions after selective micrococcal nuclease digestion. Cell. 1978 Sep;15(1):141–150. doi: 10.1016/0092-8674(78)90090-9. [DOI] [PubMed] [Google Scholar]
  8. Buongiorno-Nardelli M., Micheli G., Carri M. T., Marilley M. A relationship between replicon size and supercoiled loop domains in the eukaryotic genome. Nature. 1982 Jul 1;298(5869):100–102. doi: 10.1038/298100a0. [DOI] [PubMed] [Google Scholar]
  9. Ciejek E. M., Nordstrom J. L., Tsai M. J., O'Malley B. W. Ribonucleic acid precursors are associated with the chick oviduct nuclear matrix. Biochemistry. 1982 Sep 28;21(20):4945–4953. doi: 10.1021/bi00263a018. [DOI] [PubMed] [Google Scholar]
  10. Cockerill P. N., Garrard W. T. Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell. 1986 Jan 31;44(2):273–282. doi: 10.1016/0092-8674(86)90761-0. [DOI] [PubMed] [Google Scholar]
  11. Cohen R. B., Sheffery M. Nucleosome disruption precedes transcription and is largely limited to the transcribed domain of globin genes in murine erythroleukemia cells. J Mol Biol. 1985 Mar 5;182(1):109–129. doi: 10.1016/0022-2836(85)90031-2. [DOI] [PubMed] [Google Scholar]
  12. Cohen R. B., Sheffery M. Nucleosome disruption precedes transcription and is largely limited to the transcribed domain of globin genes in murine erythroleukemia cells. J Mol Biol. 1985 Mar 5;182(1):109–129. doi: 10.1016/0022-2836(85)90031-2. [DOI] [PubMed] [Google Scholar]
  13. Cook P. R., Brazell I. A. Conformational constraints in nuclear DNA. J Cell Sci. 1976 Nov;22(2):287–302. doi: 10.1242/jcs.22.2.287. [DOI] [PubMed] [Google Scholar]
  14. Cook P. R., Lang J., Hayday A., Lania L., Fried M., Chiswell D. J., Wyke J. A. Active viral genes in transformed cells lie close to the nuclear cage. EMBO J. 1982;1(4):447–452. doi: 10.1002/j.1460-2075.1982.tb01189.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cook P. R., Lang J. The spatial organization of sequences involved in initiation and termination of eukaryotic DNA replication. Nucleic Acids Res. 1984 Jan 25;12(2):1069–1075. doi: 10.1093/nar/12.2.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dalton S., Coleman J. R., Wells J. R. Transcription of the histone H5 gene is not S-phase regulated. Mol Cell Biol. 1986 Feb;6(2):601–606. doi: 10.1128/mcb.6.2.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Garel A., Axel R. Selective digestion of transcriptionally active ovalbumin genes from oviduct nuclei. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3966–3970. doi: 10.1073/pnas.73.11.3966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hentzen P. C., Rho J. H., Bekhor I. Nuclear matrix DNA from chicken erythrocytes contains beta-globin gene sequences. Proc Natl Acad Sci U S A. 1984 Jan;81(2):304–307. doi: 10.1073/pnas.81.2.304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Herman R., Weymouth L., Penman S. Heterogeneous nuclear RNA-protein fibers in chromatin-depleted nuclei. J Cell Biol. 1978 Sep;78(3):663–674. doi: 10.1083/jcb.78.3.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Igó-Kemenes T., Zachau H. G. Domains in chromatin structure. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 1):109–118. doi: 10.1101/sqb.1978.042.01.012. [DOI] [PubMed] [Google Scholar]
  21. Igó-Kemenes T., Zachau H. G. Domains in chromatin structure. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 1):109–118. doi: 10.1101/sqb.1978.042.01.012. [DOI] [PubMed] [Google Scholar]
  22. Jackson D. A., Cook P. R. Transcription occurs at a nucleoskeleton. EMBO J. 1985 Apr;4(4):919–925. doi: 10.1002/j.1460-2075.1985.tb03719.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jost J. P., Seldran M. Association of transcriptionally active vitellogenin II gene with the nuclear matrix of chicken liver. EMBO J. 1984 Sep;3(9):2005–2008. doi: 10.1002/j.1460-2075.1984.tb02082.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Keppel F. Transcribed human ribosomal RNA genes are attached to the nuclear matrix. J Mol Biol. 1986 Jan 5;187(1):15–21. doi: 10.1016/0022-2836(86)90402-x. [DOI] [PubMed] [Google Scholar]
  25. Krieg P. A., Robins A. J., D'Andrea R., Wells J. R. The chicken H5 gene is unlinked to core and H1 histone genes. Nucleic Acids Res. 1983 Feb 11;11(3):619–627. doi: 10.1093/nar/11.3.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lebkowski J. S., Laemmli U. K. Evidence for two levels of DNA folding in histone-depleted HeLa interphase nuclei. J Mol Biol. 1982 Apr 5;156(2):309–324. doi: 10.1016/0022-2836(82)90331-x. [DOI] [PubMed] [Google Scholar]
  27. Marsden M. P., Laemmli U. K. Metaphase chromosome structure: evidence for a radial loop model. Cell. 1979 Aug;17(4):849–858. doi: 10.1016/0092-8674(79)90325-8. [DOI] [PubMed] [Google Scholar]
  28. Miller T. E., Huang C. Y., Pogo A. O. Rat liver nuclear skeleton and ribonucleoprotein complexes containing HnRNA. J Cell Biol. 1978 Mar;76(3):675–691. doi: 10.1083/jcb.76.3.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mirkovitch J., Mirault M. E., Laemmli U. K. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell. 1984 Nov;39(1):223–232. doi: 10.1016/0092-8674(84)90208-3. [DOI] [PubMed] [Google Scholar]
  30. Molloy P. L., Powell B. C., Gregg K., Barone E. D., Rogers G. E. Organisation of feather keratin genes in the chick genome. Nucleic Acids Res. 1982 Oct 11;10(19):6007–6021. doi: 10.1093/nar/10.19.6007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Noyes B. E., Mevarech M., Stein R., Agarwal K. L. Detection and partial sequence analysis of gastrin mRNA by using an oligodeoxynucleotide probe. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1770–1774. doi: 10.1073/pnas.76.4.1770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pardoll D. M., Vogelstein B., Coffey D. S. A fixed site of DNA replication in eucaryotic cells. Cell. 1980 Feb;19(2):527–536. doi: 10.1016/0092-8674(80)90527-9. [DOI] [PubMed] [Google Scholar]
  33. Pardoll D. M., Vogelstein B. Sequence analysis of nuclear matrix associated DNA from rat liver. Exp Cell Res. 1980 Aug;128(2):466–470. doi: 10.1016/0014-4827(80)90083-x. [DOI] [PubMed] [Google Scholar]
  34. Paulson J. R., Laemmli U. K. The structure of histone-depleted metaphase chromosomes. Cell. 1977 Nov;12(3):817–828. doi: 10.1016/0092-8674(77)90280-x. [DOI] [PubMed] [Google Scholar]
  35. Powell P. C., Payne L. N., Frazier J. A., Rennie M. T lymphoblastoid cell lines from Marek's disease lymphomas. Nature. 1974 Sep 6;251(5470):79–80. doi: 10.1038/251079a0. [DOI] [PubMed] [Google Scholar]
  36. Robinson S. I., Nelkin B. D., Vogelstein B. The ovalbumin gene is associated with the nuclear matrix of chicken oviduct cells. Cell. 1982 Jan;28(1):99–106. doi: 10.1016/0092-8674(82)90379-8. [DOI] [PubMed] [Google Scholar]
  37. Robinson S. I., Small D., Idzerda R., McKnight G. S., Vogelstein B. The association of transcriptionally active genes with the nuclear matrix of the chicken oviduct. Nucleic Acids Res. 1983 Aug 11;11(15):5113–5130. doi: 10.1093/nar/11.15.5113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Ruiz-Carrillo A., Affolter M., Renaud J. Genomic organization of the genes coding for the six main histones of the chicken: complete sequence of the H5 gene. J Mol Biol. 1983 Nov 15;170(4):843–859. doi: 10.1016/s0022-2836(83)80191-0. [DOI] [PubMed] [Google Scholar]
  39. Ryoji M., Worcel A. Structure of the two distinct types of minichromosomes that are assembled on DNA injected in Xenopus oocytes. Cell. 1985 Apr;40(4):923–932. doi: 10.1016/0092-8674(85)90352-6. [DOI] [PubMed] [Google Scholar]
  40. Sittman D. B., Graves R. A., Marzluff W. F. Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1849–1853. doi: 10.1073/pnas.80.7.1849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Small D., Nelkin B., Vogelstein B. The association of transcribed genes with the nuclear matrix of Drosophila cells during heat shock. Nucleic Acids Res. 1985 Apr 11;13(7):2413–2431. doi: 10.1093/nar/13.7.2413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  43. Strätling W. H., Dölle A., Sippel A. E. Chromatin structure of the chicken lysozyme gene domain as determined by chromatin fractionation and micrococcal nuclease digestion. Biochemistry. 1986 Jan 28;25(2):495–502. doi: 10.1021/bi00350a033. [DOI] [PubMed] [Google Scholar]
  44. Swaneck G. E., Alvarez J. M. Specific binding of 3H-estradiol to rat prostate nuclear matrix. Biochem Biophys Res Commun. 1985 May 16;128(3):1381–1387. doi: 10.1016/0006-291x(85)91093-9. [DOI] [PubMed] [Google Scholar]
  45. Taniguchi T., Matsui H., Fujita T., Takaoka C., Kashima N., Yoshimoto R., Hamuro J. Structure and expression of a cloned cDNA for human interleukin-2. Nature. 1983 Mar 24;302(5906):305–310. doi: 10.1038/302305a0. [DOI] [PubMed] [Google Scholar]
  46. Weintraub H., Groudine M. Chromosomal subunits in active genes have an altered conformation. Science. 1976 Sep 3;193(4256):848–856. doi: 10.1126/science.948749. [DOI] [PubMed] [Google Scholar]
  47. Weintraub H., Larsen A., Groudine M. Alpha-Globin-gene switching during the development of chicken embryos: expression and chromosome structure. Cell. 1981 May;24(2):333–344. doi: 10.1016/0092-8674(81)90323-8. [DOI] [PubMed] [Google Scholar]
  48. Weisbrod S. Active chromatin. Nature. 1982 May 27;297(5864):289–295. doi: 10.1038/297289a0. [DOI] [PubMed] [Google Scholar]
  49. Xu M., Barnard M. B., Rose S. M., Cockerill P. N., Huang S. Y., Garrard W. T. Transcription termination and chromatin structure of the active immunoglobulin kappa gene locus. J Biol Chem. 1986 Mar 15;261(8):3838–3845. [PubMed] [Google Scholar]
  50. van Eekelen C. A., van Venrooij W. J. hnRNA and its attachment to a nuclear protein matrix. J Cell Biol. 1981 Mar;88(3):554–563. doi: 10.1083/jcb.88.3.554. [DOI] [PMC free article] [PubMed] [Google Scholar]

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