Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1984 Nov 26;12(22):8539–8551. doi: 10.1093/nar/12.22.8539

Processing and nucleo-cytoplasmic transport of histone gene transcripts.

O Georgiev, J Mous, M L Birnstiel
PMCID: PMC320397  PMID: 6095202

Abstract

Precursors of Xenopus and sea urchin histone mRNAs were synthesized in vitro with the SP6 transcription system, and their maturation and nucleo-cytoplasmic transport was studied by frog oocyte injection. 3' processing is most rapid for homologous histone messenger sequences and does not require either genuine 5' or specific 3' ends of the precursor, but capping of the 5' terminus strongly influences the efficiency of 3' processing. No generation of 5' histone mRNA ends can be detected when precursors containing 5' spacer sequence extensions are injected into the oocyte nucleus. This finding may have some implications for the question whether histone gene transcription could be polycistronic. Using a novel oocyte technique, we have separated nuclei from cytoplasm and have studied the time course of exit of the processed RNA from the oocyte nucleus into the cytoplasm. The results suggest that RNA maturation and nucleo-cytoplasmic transport are not temporally coupled processes.

Full text

PDF
8539

Images in this article

Selected References

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

  1. Berget S. M. Are U4 small nuclear ribonucleoproteins involved in polyadenylation? Nature. 1984 May 10;309(5964):179–182. doi: 10.1038/309179a0. [DOI] [PubMed] [Google Scholar]
  2. Birchmeier C., Folk W., Birnstiel M. L. The terminal RNA stem-loop structure and 80 bp of spacer DNA are required for the formation of 3' termini of sea urchin H2A mRNA. Cell. 1983 Dec;35(2 Pt 1):433–440. doi: 10.1016/0092-8674(83)90176-9. [DOI] [PubMed] [Google Scholar]
  3. Birchmeier C., Schümperli D., Sconzo G., Birnstiel M. L. 3' editing of mRNAs: sequence requirements and involvement of a 60-nucleotide RNA in maturation of histone mRNA precursors. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1057–1061. doi: 10.1073/pnas.81.4.1057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brawerman G. The Role of the poly(A) sequence in mammalian messenger RNA. CRC Crit Rev Biochem. 1981;10(1):1–38. doi: 10.3109/10409238109114634. [DOI] [PubMed] [Google Scholar]
  5. Contreras R., Cheroutre H., Degrave W., Fiers W. Simple, efficient in vitro synthesis of capped RNA useful for direct expression of cloned eukaryotic genes. Nucleic Acids Res. 1982 Oct 25;10(20):6353–6362. doi: 10.1093/nar/10.20.6353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Darnell J. E., Jr Variety in the level of gene control in eukaryotic cells. Nature. 1982 Jun 3;297(5865):365–371. doi: 10.1038/297365a0. [DOI] [PubMed] [Google Scholar]
  7. DeLeon D. V., Cox K. H., Angerer L. M., Angerer R. C. Most early-variant histone mRNA is contained in the pronucleus of sea urchin eggs. Dev Biol. 1983 Nov;100(1):197–206. doi: 10.1016/0012-1606(83)90211-7. [DOI] [PubMed] [Google Scholar]
  8. Diaz M. O., Barsacchi-Pilone G., Mahon K. A., Gall J. G. Transcripts from both strands of a satellite DNA occur on lampbrush chromosome loops of the newt Notophthalmus. Cell. 1981 Jun;24(3):649–659. doi: 10.1016/0092-8674(81)90091-x. [DOI] [PubMed] [Google Scholar]
  9. Ford J. P., Hsu M. T. Transcription pattern of in vivo-labeled late simian virus 40 RNA: equimolar transcription beyond the mRNA 3' terminus. J Virol. 1978 Dec;28(3):795–801. doi: 10.1128/jvi.28.3.795-801.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Furuichi Y., Shatkin A. J. 5'-termini of reovirus mRNA: ability of viral cores to form caps post-transcriptionally. Virology. 1977 Apr;77(2):566–578. doi: 10.1016/0042-6822(77)90482-2. [DOI] [PubMed] [Google Scholar]
  11. Galli G., Hofstetter H., Stunnenberg H. G., Birnstiel M. L. Biochemical complementation with RNA in the Xenopus oocyte: a small RNA is required for the generation of 3' histone mRNA termini. Cell. 1983 Oct;34(3):823–828. doi: 10.1016/0092-8674(83)90539-1. [DOI] [PubMed] [Google Scholar]
  12. Green M. R., Maniatis T., Melton D. A. Human beta-globin pre-mRNA synthesized in vitro is accurately spliced in Xenopus oocyte nuclei. Cell. 1983 Mar;32(3):681–694. doi: 10.1016/0092-8674(83)90054-5. [DOI] [PubMed] [Google Scholar]
  13. Grosschedl R., Birnstiel M. L. Spacer DNA sequences upstream of the T-A-T-A-A-A-T-A sequence are essential for promotion of H2A histone gene transcription in vivo. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7102–7106. doi: 10.1073/pnas.77.12.7102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hackett P. B., Traub P., Gallwitz D. The histone genes in HeLa cells are on individual transcriptional units. J Mol Biol. 1978 Dec 25;126(4):619–635. doi: 10.1016/0022-2836(78)90012-8. [DOI] [PubMed] [Google Scholar]
  15. Hagenbüchle O., Schibler U. Mouse beta-globin and adenovirus-2 major late transcripts are initiated at the cap site in vitro. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2283–2286. doi: 10.1073/pnas.78.4.2283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hentschel C. C., Birnstiel M. L. The organization and expression of histone gene families. Cell. 1981 Aug;25(2):301–313. doi: 10.1016/0092-8674(81)90048-9. [DOI] [PubMed] [Google Scholar]
  17. Hentschel C. C. Homocopolymer sequences in the spacer of a sea urchin histone gene repeat are sensitive to S1 nuclease. Nature. 1982 Feb 25;295(5851):714–716. doi: 10.1038/295714a0. [DOI] [PubMed] [Google Scholar]
  18. Hofer E., Darnell J. E., Jr The primary transcription unit of the mouse beta-major globin gene. Cell. 1981 Feb;23(2):585–593. doi: 10.1016/0092-8674(81)90154-9. [DOI] [PubMed] [Google Scholar]
  19. Kedes L. H. Histone genes and histone messengers. Annu Rev Biochem. 1979;48:837–870. doi: 10.1146/annurev.bi.48.070179.004201. [DOI] [PubMed] [Google Scholar]
  20. Krainer A. R., Maniatis T., Ruskin B., Green M. R. Normal and mutant human beta-globin pre-mRNAs are faithfully and efficiently spliced in vitro. Cell. 1984 Apr;36(4):993–1005. doi: 10.1016/0092-8674(84)90049-7. [DOI] [PubMed] [Google Scholar]
  21. Krieg P. A., Melton D. A. Formation of the 3' end of histone mRNA by post-transcriptional processing. Nature. 1984 Mar 8;308(5955):203–206. doi: 10.1038/308203a0. [DOI] [PubMed] [Google Scholar]
  22. Krämer A., Keller W., Appel B., Lührmann R. The 5' terminus of the RNA moiety of U1 small nuclear ribonucleoprotein particles is required for the splicing of messenger RNA precursors. Cell. 1984 Aug;38(1):299–307. doi: 10.1016/0092-8674(84)90551-8. [DOI] [PubMed] [Google Scholar]
  23. Lai C. J., Dhar R., Khoury G. Mapping the spliced and unspliced late lytic SV40 RNAs. Cell. 1978 Aug;14(4):971–982. doi: 10.1016/0092-8674(78)90351-3. [DOI] [PubMed] [Google Scholar]
  24. Lerner M. R., Boyle J. A., Mount S. M., Wolin S. L., Steitz J. A. Are snRNPs involved in splicing? Nature. 1980 Jan 10;283(5743):220–224. doi: 10.1038/283220a0. [DOI] [PubMed] [Google Scholar]
  25. Manley J. L., Fire A., Cano A., Sharp P. A., Gefter M. L. DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3855–3859. doi: 10.1073/pnas.77.7.3855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mauron A., Levy S., Childs G., Kedes L. Monocistronic transcription is the physiological mechanism of sea urchin embryonic histone gene expression. Mol Cell Biol. 1981 Jul;1(7):661–671. doi: 10.1128/mcb.1.7.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Moorman A. F., de Laaf R. T., Destrée O. H., Telford J., Birnstiel M. L. Histone genes from Xenopus laevis: molecular cloning and initial characterization. Gene. 1980 Aug;10(3):185–193. doi: 10.1016/0378-1119(80)90048-7. [DOI] [PubMed] [Google Scholar]
  28. Mount S. M., Pettersson I., Hinterberger M., Karmas A., Steitz J. A. The U1 small nuclear RNA-protein complex selectively binds a 5' splice site in vitro. Cell. 1983 Jun;33(2):509–518. doi: 10.1016/0092-8674(83)90432-4. [DOI] [PubMed] [Google Scholar]
  29. Nevins J. R., Blanchard J. M., Darnell J. E., Jr Transcription units of adenovirus type 2. Termination of transcription beyond the poly(A) addition site in early regions 2 and 4. J Mol Biol. 1980 Dec 15;144(3):377–386. doi: 10.1016/0022-2836(80)90096-0. [DOI] [PubMed] [Google Scholar]
  30. Nevins J. R., Darnell J. E., Jr Steps in the processing of Ad2 mRNA: poly(A)+ nuclear sequences are conserved and poly(A) addition precedes splicing. Cell. 1978 Dec;15(4):1477–1493. doi: 10.1016/0092-8674(78)90071-5. [DOI] [PubMed] [Google Scholar]
  31. Nevins J. R. The pathway of eukaryotic mRNA formation. Annu Rev Biochem. 1983;52:441–466. doi: 10.1146/annurev.bi.52.070183.002301. [DOI] [PubMed] [Google Scholar]
  32. Perry R. P. RNA processing comes of age. J Cell Biol. 1981 Dec;91(3 Pt 2):28s–38s. doi: 10.1083/jcb.91.3.28s. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rogers J., Wall R. A mechanism for RNA splicing. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1877–1879. doi: 10.1073/pnas.77.4.1877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schaffner W., Kunz G., Daetwyler H., Telford J., Smith H. O., Birnstiel M. L. Genes and spacers of cloned sea urchin histone DNA analyzed by sequencing. Cell. 1978 Jul;14(3):655–671. doi: 10.1016/0092-8674(78)90249-0. [DOI] [PubMed] [Google Scholar]
  35. Schibler U., Hagenbüchle O., Wellauer P. K., Pittet A. C. Two promoters of different strengths control the transcription of the mouse alpha-amylase gene Amy-1a in the parotid gland and the liver. Cell. 1983 Jun;33(2):501–508. doi: 10.1016/0092-8674(83)90431-2. [DOI] [PubMed] [Google Scholar]
  36. Spinelli G., Casano C., Gianguzza F., Ciaccio M., Palla F. Transcription of sea-urchin mesenchyme blastula histone genes after heat shock. Eur J Biochem. 1982 Nov 15;128(2-3):509–513. doi: 10.1111/j.1432-1033.1982.tb06994.x. [DOI] [PubMed] [Google Scholar]
  37. Wei C., Moss B. 5'-Terminal capping of RNA by guanylyltransferase from HeLa cell nuclei. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3758–3761. doi: 10.1073/pnas.74.9.3758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Yang V. W., Lerner M. R., Steitz J. A., Flint S. J. A small nuclear ribonucleoprotein is required for splicing of adenoviral early RNA sequences. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1371–1375. doi: 10.1073/pnas.78.3.1371. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES