Skip to main content
Log in

Studies on chromatin organization in a nucleolus without fibrillar centres

Presence of a sub-nucleolar structure in KCo cells of Drosophila

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

In embryonic cell-line derivative KCo of Drosophila melanogaster, the nucleolus, like most nucleoli, contains a small proportion of ribosomal DNA (1–2% of the total nucleolar DNA). The ribosomal DNA is virtually the only active gene set in the nucleolus and is found among long stretches of inactive supercoiled heterochromatic segments. We have demonstrated by use of a Feulgen-like ammine-osmium staining procedure that, depending on the state of growth, more or less fibres of decondensed DNA emanating from the intra-nucleolar chromatin (which is in continuity with the nucleolus-associated chromatin) ramify and unravel within the central nucleolar core to be transcribed. The nucleolus expands or contracts with the variation of activity and could belong to a supramolecular matricial structure such as is shown after extraction of the nuclei. After a long period of exposure to high doses of actinomycin D, the central nucleolar core became an homogeneous fibrous structure that could be interpreted as an aggregate of protein skeletal elements. The mechanism of repression and derepression of the nucleolar chromatin could thus be explained by a mechanism involving in part a sub-nucleolar structure. We propose a schematic organization of the nucleolar chromatin in KCo cells of Drosophila and discuss it in relation with other nucleolar organizations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Berezney R (1979) Dynamic properties of the nuclear matrix. In: Busch H (ed) The cell nucleus. Academic-Press, New York, vol 7, pp 413–456

    Google Scholar 

  • Berezney R, Buchholtz LA (1981) Dynamic association of replicating DNA fragments with the nuclear matrix of regenerating liver. Exp Cell Res 132:1–13

    Google Scholar 

  • Berezney R, Macaulay LK, Crane FL (1972) The purification and biochemical characterization of bovine liver nuclear membranes. J Biol Cell 247:5549–5561

    Google Scholar 

  • Bernhard W (1969) A new staining procedure for electron microscopical cytology. J Ultrastruc Res 27:250–265

    Google Scholar 

  • Bernhard W (1971) Drug induced changes in the interphase nucleus. In: Clementi F, Ceccarelli B (ed). Advances in cytopharmacology. Raven-Press, New York, vol 1, pp 49–67

    Google Scholar 

  • Brasch K (1982) Fine structure and localization of the nuclear matrix in situ. Exp Cell Res 140:161–171

    Google Scholar 

  • Burton K (1956) A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of DNA. Biochem J 62:315–321

    Google Scholar 

  • Busch H, Smetana K (1970) The nucleolus Academic Press, New York

    Google Scholar 

  • Cogliati R, Gautier A (1973) Mise en évidence de l'ADN et des polysaccharides à l'aide d'un nouveau réactif de type “Schiff”. Cr Hebd Seanc Acad Sci Paris 276:3041–3044

    Google Scholar 

  • Derenzini M, Viron A, Puvion-Dutilleul F (1982a) The Feulgenlike osmium-ammine reaction as a tool to investigate chromatin structure in thin sections. J Ultrastruct Res 80:133–147

    Google Scholar 

  • Derenzini M, Hernandez-Verdun D, Bouteille M (1982b) Visualization in situ of extended DNA filaments in nucleolar chromatin of rat hepatocytes. Exp Cell Res 141:463–468

    Google Scholar 

  • Echallier G, Ohanessian A (1970) In vitro culture of Drosophila melanogaster embryonic cells. In Vitro 6:162–172

    Google Scholar 

  • Fakan S, Puvion E (1980) The ultrastructural visualization of nucleolar and extranucleolar RNA synthesis and distribution. Int Rev Cytol 65:255–269

    CAS  PubMed  Google Scholar 

  • Franke WW, Kleinschmidt JA, Spring H, Krohne G, Grund C, Trendelenburg MF, Stoehr M, Scheer U (1981) A nucleolar skeleton of protein filaments demonstrated in amplified nucleoli of Xenopus laevis. J Cell Biol 90:285–299

    Google Scholar 

  • Gillespie D, Spiegelman S (1965) A quantitative assay for RNA/ DNA hybrids with DNA immobilized on a membrane. J Mol Biol 12:829–842

    Google Scholar 

  • Goessens G, Lepoint A (1979) The nucleolus-organizing regions (NORs): Recent data and hypothesis. Biol Cell 35:211–220

    Google Scholar 

  • Gosh S, Paweletz N, Gosh I (1978) Cytological identification and characterization of the nuclear matrix. Exp Cell Res 111:363–371

    Google Scholar 

  • Herlan G, Quevedo R, Wunderlich F (1978) Structural transformation of the nuclear matrix in situ. Exp Cell Res 115:103–110

    Google Scholar 

  • Jackson DA, McCready SJ, Cook PR (1981) RNA synthesized at the nuclear cage. Nature 292:552–555

    Google Scholar 

  • Jordan EG, McGovern JH (1982) The quantitative relationship of the fibrillar centres and other nucleolar components to changes in growth conditions, serum deprivation and low doses of actino mycin D in cultured diploid human fibroblasts. J Cell Sci 52:373–389

    Google Scholar 

  • Kaufmann SH, Coffey DS, Shaper JH (1981) Considerations in the isolation of rat liver nuclear matrix, nucleolar envelope and pore lamina complex. Exp Cell Res 132:105–113

    Google Scholar 

  • Knibiehler B, Mirre C, Rosset R (1982a) Nucleolar organizer structure and activity in a nucleolus without fibrillar centres: The nucleolus in an established Drosophila cell line. J Cell Sci 57:351–364

    Google Scholar 

  • Knibiehler B, Bernadac A, Mirre C, Rosset R (1982b) Pattern of RNA synthesis and morphological changes induced at the nucleolar level by ecdysone treatment in a Drosophila KC cell line derivative. Biol Cell 46: in press

  • Locke M, Huie P (1980) The nucleolus during epidermal development in an insect. Tissue Cell 12:175–194

    Google Scholar 

  • Mentré P (1972) Coloration sur coupes ultra-fines des acides nucléiques et de certains polysaccharides par le thallium en solution alcoolique. J Microsc 14:251–270

    Google Scholar 

  • Merriam RW (1969) Movement of cytoplasmic proteins into nuclei induced to enlarge and initiate DNA or RNA synthesis. J Cell Sci 5:333–349

    Google Scholar 

  • Mirre C, Knibiehler B (1981) Ultrastructural autoradiographic localization of the rRNA transcription sites in the quail nucleolar components using two RNA antimetabolites. Biol Cell 42:73–78

    Google Scholar 

  • Mirre C, Knibiehler B (1982) A re-evaluation of the relationships between the fibrillar centres and the nucleolus-organizing-regions in reticulated nucleoli: ultrastructural organization, number and distribution of the fibrillar centres in the nucleolus of the mouse Sertoli cell. J Cell Sci 55:247–259

    Google Scholar 

  • Mirre C, Stahl A (1978) Peripheral RNA synthesis of fibrillar centres in nucleoli of Japanese quail oocytes and somatic cells. J Ultrastruct Res 64:377–387

    Google Scholar 

  • Mirre C, Stahl A (1981) Ultrastructural organization, sites of transcription and distribution of fibrillar centres in the nucleolus of the mouse oocyte. J Cell Sci 48:105–126

    Google Scholar 

  • Recher L, Whitescarver J, Briggs LG (1969) Fine ultrastructure of a nucleolar constituent. J Ultrastruct Res 29:1–14

    Google Scholar 

  • Ritossa MF, Spiegelman S (1965) Localization of DNA complementary to rRNA in the nucleolus organizer region of Drosophila melanogaster. Proc Natl Acad Sci USA 53:737–745

    Google Scholar 

  • Rodman TC (1969) Morphology and replication of intranucleolar DNA in polytene nuclei. J Cell Biol 42:575–582

    Google Scholar 

  • Todorov IT, Hadjiolov AA (1979) A comparison of nuclear and nucleolar matrix proteins from rat liver. Cell Biol Int Rep 3:753–757

    Google Scholar 

  • Unuma T, Senda R, Muramatsu M (1972) Mechanism of nucleolar segregation. Differences in effects of Actinomycin D and Cycloheximide on nucleoli of rat liver cells. J Electron Microsc 22:205–216

    Google Scholar 

  • Van Eekelen CAG, Salden MHL, Habets WJA, Van de Putte LBA, Van Vendrooij WJ (1982) On the existence of an internal nuclear protein structure in HeLa cells. Exp Cell Res 141:181–190

    Google Scholar 

  • Wachtler F, Ellinger A, Schwarzacher HG (1980) Nucleolar changes in human phytohaemagglutinin stimulated lymphocytes. Cell Tissue Res 213:351–360

    Google Scholar 

  • Wunderlich F, Berezney R, Kleinig H (1976) The nuclear envelope: an interdisciplinary analysis of its morphology, composition and functions. In: Chapman D, Wallach DFH (eds). Biological membranes. Academic-Press, New York, vol 3, pp 241–333

    Google Scholar 

  • Zalta J, Zalta J-P (1973) Basic principles of a method of nucleoli isolation. In: Prescott DM (ed) Methods in cell biology. Academic-Press, New York, vol 6, pp 317–330

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Knibiehler, B., Mirre, C., Navarro, A. et al. Studies on chromatin organization in a nucleolus without fibrillar centres. Cell Tissue Res. 236, 279–288 (1984). https://doi.org/10.1007/BF00214228

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00214228

Key words

Navigation