Abstract
The round nucleoli of chick embryo fibroblast cells, when exposed to adenosine (2 mM)or to a number of adenosine analogues, lose material and unravel over a period of several hours to become beaded strands, 20 mu M in length, termed nucleolar necklaces (NN). Light microscope observations on this process are described. Biochemical experiments have revealed that most of these analogues interfere with both messenger RNA synthesis and ribosome synthesis, causing extensive degradation of the preribosome species containing 32S RNA although most of the preribosomes containing 18S RNA survive. We suggest that it is the depletion from the nucleolus of the adhesive 32S and 28S RNA preribosomes which allows the remaining nucleolar apparatus to spread apart into the NN configuration. Also required for the maintenance of the NN structure is the synthesis of some ribosomal RNA (rRNA) possibly present as rRNA "feathers" on the DNA. The addition of inhibitors of rRNA synthesis such as actinomycin D to the NN-containing cells causes loss of rRNA. Then a contraction and collapse of the NN structure into small dense spheres is observed.
Full Text
The Full Text of this article is available as a PDF (2.8 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Attardi G., Amaldi F. Structure and synthesis of ribosomal RNA. Annu Rev Biochem. 1970;39:183–226. doi: 10.1146/annurev.bi.39.070170.001151. [DOI] [PubMed] [Google Scholar]
- Brdar B., Rifkin D. B., Reich E. Studies of Rous sarcoma virus. Effects of nucleoside analogues on virus synthesis. J Biol Chem. 1973 Apr 10;248(7):2397–2408. [PubMed] [Google Scholar]
- Byers B. Structure and formation of ribosome crystals in hypothermic chick embryo cells. J Mol Biol. 1967 Jun 14;26(2):155–167. doi: 10.1016/0022-2836(67)90288-4. [DOI] [PubMed] [Google Scholar]
- Granick D. Nucleolar necklaces in chick embryo fibroblast cells. I. Formation of necklaces by dichlororibobenzimidazole and other adenosine analogues that decrease RNA synthesis and degrade preribosomes. J Cell Biol. 1975 May;65(2):398–417. doi: 10.1083/jcb.65.2.398. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Granick S., Granick D. Nucleolar necklaces in chick embryo myoblasts formed by lack of arginine. J Cell Biol. 1971 Dec;51(3):636–642. doi: 10.1083/jcb.51.3.636. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Granick S. The induction in vitro of the synthesis of delta-aminolevulinic acid synthetase in chemical porphyria: a response to certain drugs, sex hormones, and foreign chemicals. J Biol Chem. 1966 Mar 25;241(6):1359–1375. [PubMed] [Google Scholar]
- Heine U. Electron microscopic studies on HeLa cells exposed to the antibiotic toyocamycin. Cancer Res. 1969 Oct;29(10):1875–1880. [PubMed] [Google Scholar]
- Jacob S. T., Muecke W., Sajdel E. M., Munro H. N. Evidence for extranucleolar control of RNA synthesis in the nucleolus. Biochem Biophys Res Commun. 1970 Jul 27;40(2):334–342. doi: 10.1016/0006-291x(70)91014-4. [DOI] [PubMed] [Google Scholar]
- Lettré R., Siebs W., Paweletz N. Morphological observations on the nucleolus of cells in tissue culture, with special regard to its composition. Natl Cancer Inst Monogr. 1966 Dec;23:107–123. [PubMed] [Google Scholar]
- Miller O. L., Jr, Beatty B. R. Visualization of nucleolar genes. Science. 1969 May 23;164(3882):955–957. doi: 10.1126/science.164.3882.955. [DOI] [PubMed] [Google Scholar]
- Monneron A., Burglen J., Bernhard W. Action of toyocamycin on nucleolar fine structure and function. J Ultrastruct Res. 1970 Aug;32(3):370–389. doi: 10.1016/s0022-5320(70)80016-8. [DOI] [PubMed] [Google Scholar]
- Phillips S. G., Phillips D. M. Nucleoli of diploid cell strains. Thei normal ultrastructure and the effects of toyocamycin and actinomycin D. J Cell Biol. 1971 Jun;49(3):785–802. doi: 10.1083/jcb.49.3.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Recher L. Fine structural changes in the nucleus induced by adenosine. J Ultrastruct Res. 1970 Aug;32(3):212–225. doi: 10.1016/s0022-5320(70)80002-8. [DOI] [PubMed] [Google Scholar]
- Siev M., Weinberg R., Penman S. The selective interruption of nucleolar RNA synthesis in HeLa cells by cordycepin. J Cell Biol. 1969 May;41(2):510–520. doi: 10.1083/jcb.41.2.510. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sverak L., Bonar R. A., Langlois A. J., Beard J. W. Inhibition by toyocamycin of RNA synthesis in mammalian cells and in normal and avian tumor virus-infected chick embryo cells. Biochim Biophys Acta. 1970 Dec 14;224(2):441–450. doi: 10.1016/0005-2787(70)90576-9. [DOI] [PubMed] [Google Scholar]
- TAMIR H., RATNER S. A STUDY OF ORNITHINE, CITRULLINE AND ARGININE SYNTHESIS IN GROWING CHICKS. Arch Biochem Biophys. 1963 Aug;102:259–269. doi: 10.1016/0003-9861(63)90179-6. [DOI] [PubMed] [Google Scholar]
- Taddei C. Ribosome arrangement during oogenesis of Lacerta sicula Raf. Exp Cell Res. 1972 Feb;70(2):285–292. doi: 10.1016/0014-4827(72)90138-3. [DOI] [PubMed] [Google Scholar]
- Tata J. R., Hamilton M. J., Shields D. Effects of alpha-amanitin in vivo on RNA polymerase and nuclear RNA synthesis. Nat New Biol. 1972 Aug 9;238(84):161–164. doi: 10.1038/newbio238161a0. [DOI] [PubMed] [Google Scholar]
- Tavitian A., Uretsky S. C., Acs G. Selective inhibition of ribosomal RNA synthesis in mammalian cells. Biochim Biophys Acta. 1968 Mar 18;157(1):33–43. doi: 10.1016/0005-2787(68)90261-x. [DOI] [PubMed] [Google Scholar]
- Wellauer P. K., Dawid I. B. Secondary structure maps of RNA: processing of HeLa ribosomal RNA. Proc Natl Acad Sci U S A. 1973 Oct;70(10):2827–2831. doi: 10.1073/pnas.70.10.2827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willems M., Penman M., Penman S. The regulation of RNA synthesis and processing in the nucleolus during inhibition of protein synthesis. J Cell Biol. 1969 Apr;41(1):177–187. doi: 10.1083/jcb.41.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]