Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1980 Jul 25;8(14):3087–3103. doi: 10.1093/nar/8.14.3087

Post-transcriptional regulation of messenger abundance in rat liver and hepatoma.

H Jacobs, G D Birnie
PMCID: PMC324357  PMID: 6108552

Abstract

Saturation hybridisation with labelled single-copy DNA shows that polysomal poly(A)+ RNA of rat liver and of a minimum-deviation rat hepatoma cell-line (HTC) have similar total complexities and that few sequences are specific to either cell-type. Hybridisation kinetics of polysomal cDNAs with template and heterologous cell RNAs indicate that a proportion of liver messengers are at greatly reduced abundance in the hepatoma, but not the converse. Hybridisations using fractionated cDNAs enriched for abundant polysomal sequences confirm these findings: on average, abundant liver mRNAs are about 100-fold rarer in hepatoma, whereas abundant hepatoma mRNAs are only 5-fold rarer in liver. This pattern is also implied by cell-free translation of polysomal poly(A)+ RNAs. The reactions of total and fractionated polysomal cDNA probes with poly(A)+ nuclear RNA indicate that there is much less disparity in abundance of these sequences at nuclear level, implying that the differences arise, at least in part, post-transcriptionally. We interpret the altered mRNA abundances in the hepatoma in terms both of its decreased functional specialisation and its ability to proliferate.

Full text

PDF
3087

Images in this article

Selected References

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

  1. Affara N. A., Jacquet M., Jakob H., Jacob F., Gros F. Comparison of polysomal polyadenylated RNA from embryonal carcinoma and committed myogenic and erythropoietic cell lines. Cell. 1977 Oct;12(2):509–520. doi: 10.1016/0092-8674(77)90127-1. [DOI] [PubMed] [Google Scholar]
  2. Anderson C. W., Baum P. R., Gesteland R. F. Processing of adenovirus 2-induced proteins. J Virol. 1973 Aug;12(2):241–252. doi: 10.1128/jvi.12.2.241-252.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Axel R., Feigelson P., Schutz G. Analysis of the complexity and diversity of mRNA from chicken liver and oviduct. Cell. 1976 Feb;7(2):247–254. doi: 10.1016/0092-8674(76)90024-6. [DOI] [PubMed] [Google Scholar]
  5. BUCHER N. L. REGENERATION OF MAMMALIAN LIVER. Int Rev Cytol. 1963;15:245–300. doi: 10.1016/s0074-7696(08)61119-5. [DOI] [PubMed] [Google Scholar]
  6. Church R., McCarthy B. J. Changes in nuclear and cytoplasmic RNA in regenerating mouse liver. Proc Natl Acad Sci U S A. 1967 Oct;58(4):1548–1555. doi: 10.1073/pnas.58.4.1548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davidson E. H., Britten R. J. Regulation of gene expression: possible role of repetitive sequences. Science. 1979 Jun 8;204(4397):1052–1059. doi: 10.1126/science.451548. [DOI] [PubMed] [Google Scholar]
  8. Galau G. A., Klein W. H., Davis M. M., Wold B. J., Britten R. J., Davidson E. H. Structural gene sets active in embryos and adult tissues of the sea urchin. Cell. 1976 Apr;7(4):487–505. doi: 10.1016/0092-8674(76)90200-2. [DOI] [PubMed] [Google Scholar]
  9. Gamulin S., Gray C. H., Norman M. R. Comparison of methods for preparing polysomes free of glycogen. Biochim Biophys Acta. 1972 Jan 31;259(2):239–242. doi: 10.1016/0005-2787(72)90063-9. [DOI] [PubMed] [Google Scholar]
  10. Getz M. J., Birnie G. D., Young B. D., MacPhail E., Paul J. A kinetic estimation of base sequence complexity of nuclear poly(A)-containing RNA in mouse Friend cells. Cell. 1975 Feb;4(2):121–129. doi: 10.1016/0092-8674(75)90118-x. [DOI] [PubMed] [Google Scholar]
  11. Getz M. J., Reiman H. M., Jr, Siegal G. P., Quinlan T. J., Proper J., Elder P. K., Moses H. L. Gene expression in chemically transformed mouse embryo cells: selective enhancement of the expression of C type RNA tumor virus genes. Cell. 1977 Aug;11(4):909–921. doi: 10.1016/0092-8674(77)90302-6. [DOI] [PubMed] [Google Scholar]
  12. Graf T., Beug H. Avian leukemia viruses: interaction with their target cells in vivo and in vitro. Biochim Biophys Acta. 1978 Nov 17;516(3):269–299. doi: 10.1016/0304-419x(78)90011-2. [DOI] [PubMed] [Google Scholar]
  13. Greaves M., Janossy G. Patterns of gene expression and the cellular origins of human leukaemias. Biochim Biophys Acta. 1978 Oct 27;516(2):193–230. doi: 10.1016/0304-419x(78)90008-2. [DOI] [PubMed] [Google Scholar]
  14. Harpold M. M., Evans R. M., Salditt-Georgieff M., Darnell J. E. Production of mRNA in Chinese hamster cells: relationship of the rate of synthesis to the cytoplasmic concentration of nine specific mRNA sequences. Cell. 1979 Aug;17(4):1025–1035. doi: 10.1016/0092-8674(79)90341-6. [DOI] [PubMed] [Google Scholar]
  15. Hunt J. A. Rate of synthesis and half-life of globin messenger ribonucleic acid. Rate of synthesis of globin messenger ribonucleic acid calculated from data of cell haemoglobin content. Biochem J. 1974 Mar;138(3):499–510. doi: 10.1042/bj1380499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hynes N. E., Groner B., Sippel A. E., Nguyen-Huu M. C., Schütz G. mRNA complexity and egg white protein mRNA content in mature and hormone-withdrawn oviduct. Cell. 1977 Aug;11(4):923–932. doi: 10.1016/0092-8674(77)90303-8. [DOI] [PubMed] [Google Scholar]
  17. Kleiman L., Birnie G. D., Young B. D., Paul J. Comparison of the base-sequence complexities of polysomal and nuclear RNAs in growing Friend erythroleukemia cells. Biochemistry. 1977 Mar 22;16(6):1218–1223. doi: 10.1021/bi00625a029. [DOI] [PubMed] [Google Scholar]
  18. Knöchel W., Patel N. T., Holoubek V. Polysomal poly(A)+ RNA in liver of rats fed 3'-methyl-4-dimethylaminoazobenzene and in hepatoma induced by the same carcinogen. Biochim Biophys Acta. 1980;606(1):67–75. doi: 10.1016/0005-2787(80)90098-2. [DOI] [PubMed] [Google Scholar]
  19. Lowenhaupt K., Lingrel J. B. A change in the stability of globin mRNA during the induction of murine erythroleukemia cells. Cell. 1978 Jun;14(2):337–344. doi: 10.1016/0092-8674(78)90119-8. [DOI] [PubMed] [Google Scholar]
  20. Parker M. G., Mainwaring W. I. Effects of androgens on the complexity of poly(A) RNA from rat prostate. Cell. 1977 Oct;12(2):401–407. doi: 10.1016/0092-8674(77)90116-7. [DOI] [PubMed] [Google Scholar]
  21. Paul J., Zollner E. J., Gilmour R. S., Birnie G. D. Properties of transcriptionally active chromatin. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 1):597–603. doi: 10.1101/sqb.1978.042.01.062. [DOI] [PubMed] [Google Scholar]
  22. Pelham H. R., Jackson R. J. An efficient mRNA-dependent translation system from reticulocyte lysates. Eur J Biochem. 1976 Aug 1;67(1):247–256. doi: 10.1111/j.1432-1033.1976.tb10656.x. [DOI] [PubMed] [Google Scholar]
  23. Reel J. R., Kenney F. T. "Superinduction" of tyrosine transaminase in hepatoma cell cultures: differential inhibition of synthesis and turnover by actionomycin D. Proc Natl Acad Sci U S A. 1968 Sep;61(1):200–206. doi: 10.1073/pnas.61.1.200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rolton H. A., Birnie G. D., Paul J. The diversity and specificity of nuclear and polysomal poly(A)+ RNA populations in normal and MSV-transformed cells. Cell Differ. 1977 Jun;6(1):25–39. doi: 10.1016/0045-6039(77)90042-2. [DOI] [PubMed] [Google Scholar]
  25. Savage M. J., Sala-Trepat J. M., Bonner J. Measurement of the complexity and diversity of poly(adenylic acid) containing messenger RNA from rat liver. Biochemistry. 1978 Feb 7;17(3):462–467. doi: 10.1021/bi00596a014. [DOI] [PubMed] [Google Scholar]
  26. Shearer R. W., Smuckler E. A. Altered regulation of the transport of RNA from nucleus to cytoplasm in rat hepatoma cells. Cancer Res. 1972 Feb;32(2):339–342. [PubMed] [Google Scholar]
  27. Thompson E. B., Tomkins G. M., Curran J. F. Induction of tyrosine alpha-ketoglutarate transaminase by steroid hormones in a newly established tissue culture cell line. Proc Natl Acad Sci U S A. 1966 Jul;56(1):296–303. doi: 10.1073/pnas.56.1.296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wilkes P. R., Birnie G. D., Paul J. Changes in nuclear and polysomal polyadenylated RNA sequences during rat-liver regeneration. Nucleic Acids Res. 1979;6(6):2193–2208. doi: 10.1093/nar/6.6.2193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Williams J. G., Penman S. The messenger RNA sequences in growing and resting mouse fibroblasts. Cell. 1975 Oct;6(2):197–206. doi: 10.1016/0092-8674(75)90010-0. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES